Abstract
Molecular markers based upon a novel lettuce LTR retrotransposon and the nucleotide binding site-leucine-rich repeat (NBS-LRR) family of disease resistance-associated genes have been combined with AFLP markers to generate a 458 locus genetic linkage map for lettuce. A total of 187 retrotransposon-specific SSAP markers, 29 NBS-LRR markers and 242 AFLP markers were mapped in an F2 population, derived from an interspecific cross between a Lactuca sativa cultivar commonly used in Europe and a wild Lactuca serriola isolate from Northern Europe. The cross has been designed to aid efforts to assess gene flow from cultivated lettuce into the wild in the perspective of genetic modification biosafety. The markers were mapped in nine major and one minor linkage groups spanning 1,266.1 cM, with an average distance of 2.8 cM between adjacent mapped markers. The markers are well distributed throughout the lettuce genome, with limited clustering of different marker types. Seventy-seven of the AFLP markers have been mapped previously and cross-comparison shows that the map from this study corresponds well with the previous linkage map.
Similar content being viewed by others
References
Bernatsky R, Tanksley SD (1989) Restriction fragments as molecular markers for germplasm evaluation and utilisation. In: Brown AHD, et al. (eds) The use of plant genetic resources. Cambridge University Press, Cambridge, pp 353–362
Calenge F, Van der Linden CG, Van de Weg E, Schouten HJ, Van Arkel G, Denancé C, Durel CE (2005) Resistance gene analogues identified through the NBS-profiling method map close to major genes and QTL for disease resistance in apple. Theor Appl Genet 110:660–668
Casa AM, Brouwer C, Nagel A, Wang L, Zhang Q, Kresovich S, Wessler SR (2000) Inaugural article: the MITE family heartbreaker (Hbr): molecular markers in maize. Proc Natl Acad Sci USA 97:10083–10089
Castiglioni P, Ajmone-Marsan P, Wijk R (1999) AFLP markers in a molecular linkage map of maize: codominant scoring and linkage group distribution. Theor Appl Genet 99:425–431
Ellis TH, Poyser SJ, Knox MR, Vershinin AV, Ambrose MJ (1998) Ty1- copia class retrotransposon insertion site polymorphism for linkage and diversity analysis in pea. Mol Gen Genet 260:9–19
Flavell AJ, Knox MR, Pearce SR, Ellis TH (1998) Retrotransposon-based insertion polymorphisms (RBIP) for high throughput marker analysis. Plant J 16:643–650
Gray AJ (2004) Ecology and government politics: the GM crop debate. J Appl Ecol 41:1–10
Gribbon BM, Pearce SR, Kalendar R, Schulman AH, Paulin L, Jack P, Kumar A, Flavell AJ (1999) Phylogeny and transpositional activity of Ty1-copia group retrotransposons in cereal genomes. Mol Gen Genet 261:883–891
Hails RS (2000) Genetically modified plants—the debate continues. Trends Ecol Evol 15:14–18
Haanstra JPW, Wye C, Verbakel H, Meijer-Dekens F, Van den Berg P, Odinot P, Van Heusden AW, Tanksley S, Lindhout P, Peleman P (1999) An integrated high-density RFLP-AFLP map of tomato based on two Lycopersicon esculentum •L. pennellii F 2 populations. Theor Appl Genet 99:254–271
Hooftman DAP, Oostermeijer JGB, Jacobs M, Den Nijs HCM (2005) Demographic vital rates determine the performance advantage of crop-wild hybrids in Lettuce. J Appl Ecol (in press)
Jeuken M, van Wijk R, Peleman P, Lindhout P (2001) An integrated interspecific AFLP map of lettuce (Lactuca) based on two L. sativa ¥ L. saligna F2 populations. Theor Appl Genet 103:638–647
Kesseli RV, Paran I, Michelmore RW (1994) Analysis of a detailed genetic linkage map of Lactuca sativa (Lettuce) constructed from RFLP and RAPD markers. Genetics 136:1435–1446
Klein PE, Klein RR, Cartinhour SW, Ulanch PE, Dong J, Obert JA, Morishige DT, Schlueter SD, Childs KL, Ale M, Mullet JE (2000) A high-throughput AFLP-based method for constructing integrated genetic and physical maps: progress toward a sorghum genome map. Genome Res 10:789–807
Knapp SJ (1998) Marker-assisted selection as a strategy for increasing the probability of selecting superior genotypes. Crop Sci 38:1164–1174
Korswagen HC, Durbin RM, Smits MT, Plasterk RHA (1996) Transposon Tc1-derived, sequence-tagged sites in Caenorhabditis elegans as markers for gene mapping. Proc Natl Acad Sci USA 93:14680–14685
Kosambi DD (1943) The estimation of map units from recombination values. Ann Eugen 12:172–175
Lande R, Thompson R (1990) Efficiency of markers—assisted selection in the improvement of quantitative traits. Genetics 124:743–756
Leigh F, Kalendar R, Lea V, Lee D, Donini P, Schulman AH (2003) Comparison of the utility of barley retrotransposon families for genetic analysis by molecular marker techniques. Mol Genet Genomics 269:464–474
Mantovani P, van der Linden G, Maccaferri M, Sanguineti MC, Tuberosa R (2004) Molecular characterization of durum wheat germplasm with NBS markers as compared to AFLPs and SSRs. In: Vollmann J, Grausgruber H, Ruckenbauer P (eds) Proceedings of 17th EUCARPIA General congress: genetic variation for plant breeding. University of Natural Resources and Applied Life Sciences, Vienna, pp 146
Mei M, Syed NH, Gao W, Thaxton P, Stelly D, Chen ZJ (2004) Genetic mapping and QTL analysis of fiber-related traits in cotton (Gossypium). Theor Appl Genet 108:280–291
Meyers BC, Chin DB, Shen KA, Sivaramakrishnan S, Lavelle DO, Zhang Z, Michelmore RW (1998) The major resistance gene cluster in lettuce is highly duplicated and spans several megabases. Plant Cell 10:1817–1832
Nagata RT (1992) Clip-and-wash method of emasculation for lettuce. Hortiscience 27:907–908
Pearce SR, Stuart-Rogers C, Knox MR, Kumar A, Ellis TH, Flavell AJ (1999) Rapid isolation of plant Ty1-copia group retrotransposon LTR sequences for molecular marker studies. Plant J 19:711–717
Pearce SR, Knox M, Ellis THN, Flavell AJ, Kumar A (2000) Pea Ty1-copia group retrotransposons: transpositional activity and use as markers to study genetic diversity in Pisum. Mol Gen Genet 263:898–907
Porceddu A, Albertini E, Barcaccia G, Marconi G, Bertoli FB, Veronesi F (2002) Development of S-SAP markers based on an LTR-like sequence from Medicago sativa L. Mol Genet Genomics 267:107–114
Qi X, Stam P, Lindhout P (1998) Use of locus-specific AFLP markers to construct a high-density molecular map in barley. Theor Appl Genet 96:376–384
Queen RA, Gribbon BM, James C, Jack P, Flavell AJ (2004). Retrotransposon-based molecular markers for linkage and genetic diversity analysis in wheat. Mol Genet Genomics 271:91–97
Reeves JC, Chiapparino, E Donini P, Ganal M, Guiard J, Hamrit S, Heckenberger M, Huang X-Q, van Kaauwen M, Kochieva E, Koebner R, Law JR, Lea V, LeClerc V, van der Lee T, Leigh F, van der Linden G, Malysheva L, Melchinger AE, Orford S, Reif JC, Röder M, Schulman A, Vosman B, van der Wiel C, Wolf M, Zhang D (2004) Changes over time in the genetic diversity of four major European crops from the Gediflux Framework 5 project. In: Vollmann J, Grausgruber H, Ruckenbauer P (eds) Proceedings of 17th EUCARPIA General congress: genetic variation for plant breeding. University of Natural Resources and Applied Life Sciences, Vienna, pp 3–7
Ryder EJ (1999) Lettuce, Endive and Chicory. CAB International, Wallingford
Sebastian RL, Howell EC, King GJ, Marshall DF, Kearsey MJ (2000) An integrated AFLP and RFLP Brassica oleracea linkage map from two morphologically distinct doubled-haploid mapping populations. Theor Appl Genet 100:75–81
Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA 81:8014–8018
Schulman AH, Flavell AJ, Ellis THN (2004) The application of LTR retrotransposons as genetic markers in plants. In: Miller W, Capy P (eds) Mobile genetic elements: protocols and genomic applications. Humana Press Inc, Totowa,
Snow AA, Andow DA, Gepts P, Hallerman EM, Power A, Tiedje JM, Wolfenbarger LL (2005) Genetically engineered organisms and the environment: current status and recommendations. Ecol Appl 15:377–404
Stam P, Van Ooijen JW (1995) JoinMap version 2.0: software for the calculation of genetic linkage maps. PRI-DLO, Wageningen
Syed NH, Sureshsundar S, Wilkinson MJ, Bhau BS, Cavalcanti JJV, Flavell AJ (2005) Ty1-copia retrotransposon-based SSAP marker development in Cashew (Anacardium occidentale L.). Theor Appl Genet 110:1195–1202
Van de Wiel C , Van der Linden G , Hans den Nijs, Flavell AJ, Syed N , Jorgensen R, Felber F , Scotti I, Van der Voort JR Peleman J (2003) An EU project on gene flow analysis between crop and wild forms of lettuce and chicory. In: van Hintum ThJL, Lebeda A, Pink D, Schut JW (eds) The context of GMO biosafety: Eucarpia leafy vegetables
Van der Linden CG, Wouters DCAE, Mihalka V, Kochieva EZ, Smulders MJM, Vosman B (2004) Efficient targeting of plant disease resistance loci using NBS profiling. Theor Appl Genet 109:384–393
Virk PS, Pooni HS, Syed NH, Kearsey MJ (1999) Fast and reliable genotype validation using microsatellite markers in Arabidopsis thaliana. Theor Appl Genet 98:462–464
Voorrips RE (2002) MapChart, Software for the graphical presentation of linkage maps and QTLs. J Heredity 93:77–78
Vuylsteke M, Mank R, Antonise R, Bastiaans E, Senior ML, Stuber CW, Melchinger AE, Lübberstedt T, Xia XC, Stam P, Zabeau M, Kuiper M (1999) Two high-density AFLP linkage maps of Zea mays L.: analysis of distribution of AFLP markers. Theor Appl Genet 99:921–935
Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414
Waugh R, McLean K, Flavell AJ, Pearce SR, Kumar A, Thomas BB, Powell W (1997) Genetic distribution of BARE-1-like retrotransposable elements in the barley genome revealed by sequence-specific amplification polymorphisms (S-SAP). Mol Gen Genet 253:687–694
Young WP, Schupp JM, Keim P (1999) DNA methylation and AFLP marker distribution in the soybean genome. Theor Appl Genet 99:785–792
Yu GX, Wise RP (2000) An anchored AFLP- and retrotransposon-based map of diploid Avena. Genome 43:736–749
Acknowledgements
This work was supported by Grant 01657 (ANGEL) from the European Commission under the Frameworks VI Programme. We are very grateful to Richard Michelmore, Maria Truco and Alex Kozic who generously provided us with lettuce EST data filtered for transposon sequences prior to publication, together with much helpful advice on linkage mapping in lettuce. We are also thankful for many interesting and fruitful discussions from the other members of the ANGEL partnership—Rikke Bagger Jørgensen, François Felber, Jeroen Rouppe Van der Voort, Gerard Ostermeier and Massimo Vischi.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J. S. Heslop-Harrison
Rights and permissions
About this article
Cite this article
Syed, N.H., Sørensen, A.P., Antonise, R. et al. A detailed linkage map of lettuce based on SSAP, AFLP and NBS markers. Theor Appl Genet 112, 517–527 (2006). https://doi.org/10.1007/s00122-005-0155-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-005-0155-4