Abstract
Sugar beet (Beta vulgaris) is an important root crop for sucrose production. A study was conducted to find a new abundant source of microsatellite (SSR) markers in order to develop marker assistance for breeding. Different sources of existing microsatellites were used and new ones were developed to compare their efficiency to reveal diversity in mapping population and mapping coverage. Forty-one microsatellite markers were isolated from a B. vulgaris ssp maritima genomic library and 201 SSRs were extracted from a B. vulgaris ssp vulgaris library. Data mining was applied on GenBank B. vulgaris expressed sequence tags (ESTs), 803 EST-SSRs were identified over 19,709 ESTs. Characteristics, polymorphism and cross-species transferability of these microsatellites were compared. Based on these markers, a high density genetic map was constructed using 92 F2 individuals from a cross between a sugar and a table beet. The map contains 284 markers, spans over 555 cM and covers the nine chromosomes of the species with an average markers density of one marker every 2.2 cM. A set of markers for assignation to the nine chromosomes of sugar beet is provided.
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Andersen NS, Siegismund HR, Meyer V, Jorgensen RB (2005) Low level of gene flow from cultivated beets (Beta vulgaris L. ssp vulgaris) into Danish populations of sea beet (Beta vulgaris L. ssp. maritima (L.) Arcangeli). Mol Ecol 14:1391–1405
Arnaud JF, Viard F, Delescluse M, Cuguen J (2003) Evidence for gene flow via seed dispersal from crop to wild relatives in Beta vulgaris (Chenopodiaceae): consequences for the release of genetically modified crop species with weedy lineages. Proc R Soc Lond 1524:1565–1571
Areshchenkova T, Ganal M (2002) Comparative analysis of polymorphism and chromosomal location of tomato microsatellite markers isolated from three different sources. Theor Appl Genet 104:229–235
Barzen E, Mechelke W, Ritter E, Seitzer J, Salamini F (1992) RFLP markers for sugar beet breeding: chromosomal linkage maps and location of major genes for rhizomania resistance, monogermy and hypocotyl colour. Plant J 2:601–611
Barzen E, Mechelke W, Ritter E, Schulte-Kappert E, Salamini F (1995) An extended map of the sugar beet genome containing RFLP and RAPD loci. Theor Appl Genet 90:189–193
Barzen E, Stahl R, Fuchs E, Borchardt D, Salamini F (1997) Development of coupling-repulsion-phase SCAR markers diagnostic for the sugar beet Rr1 allele conferring resistance to rhizomania. Mol Breed 3:231–238
Boudry P, Wieber R, Saumitou-Laprade P, Pillen K, VanDijk H, Jung C (1994) Identification of RFLP markers closely linked to the bolting gene B and their significance for the study of the annual habit in beets (Beta vulgaris L.). Theor Appl Genet 88:852–858
Butterfass T (1964) Die chloroplastenzahlen in verschiedenartigen zellen trisomer zuckerruben (Beta vulgaris L.). Z Bot 52:46–77
Butterfass T (1968) Die Zuordnung des Locus R der Zuckerrübe (Hypokotylfarbe) zum Chromosom II. Theor Appl Genet 38:348–350
Cardle L, Ramsay L, Milbourne D, Macaulay M, Marshall D, Waugh R (2000) Computational and experimental characterization of physically clustered simple sequence repeats in plants. Genetics 156:847–854
Cho Y, Ishii T, Temnykh S, Chen X, Lipovich L, McCouch S, Park W, Ayres N, Cartinhour S (2000) Diversity of microsatellites derived from genomic libraries and GenBank sequences in rice (Oryza sativa L.). Theor Appl Genet 100:713–722
Cureton A, Burns M, Ford-Lloyd B, Newbury H (2002) Development of simple sequence repeat (SSR) markers for the assesment of gene flow between sea beet (Beta vulgaris ssp. maritima) populations. Mol Ecol Note 2:402–403
Decroocq V, Fave M, Hagen L, Bordenave L, Decroocq S (2003) Development and transferability of apricot and grape EST microsatellite markers across taxa. Theor Appl Genet 106:912–922
El-Mezawy A, Dreyer F, Jacobs G, Jung C (2002) High-resolution mapping of the mapping gene B of sugar beet. Theor Appl Genet 105:100–105
Eujayl I, Sorrells M, Baum M, Wolters P, Powell W (2001) Assessment of genotypic variation among cultivated durum wheat based on EST-SSRS and genomic SSRS. Euphytica 119:39–43
Friesen T, Weiland J, Aasheim M, Hunger S, Borchardt D, Lewellen R (2006) Identification of a SCAR marker associated with B m, the beet mosaic virus resistance gene, on chromosome 1 of sugar beet. Plant Breed 125:167–172
Fujimori S, Washio T, Higo K, Ohtomo Y, Murakami K, Matsubara K, Kawai J, Carninci P, Hayashizaki Y, Kikuchi S, Tomita M (2003) A novel feature of microsatellites in plants: a distribution gradient along the direction of transcription. FEBS Lett 554:17–22
Guo W, Wang W, Zhou B, Zhang T (2006) Cross-species transferability of G. arboreum-derived EST-SSRs in the diploid species of Gossypium. Theor Appl Genet 112:1573–1581
Hackauf B, Wehling P (2002) Identification of microsatellite polymorphisms in a expressed portion of the rye genome. Plant Breed 121:17–25
Hagihara E, Matsuhira H, Ueda M, Mikami T, Kubo T (2005) Sugar beet BAC library construction and assembly of a contig spanning Rf1, a restorer-of-fertility gene for Owen cytoplasmic male sterility. Mol Genet Genomics 4:1–8
Halldén C, Hjerdin A, Rading I, Säll T, Fridlundh B, Johannisdottir G, Tuvesson S, Akesson C, Nilsson N (1996) A high density RFLP linkage map of sugar beet. Genome 39:634–645
Hirata M, Cai H, Inoue M, Yuyama N, Miura Y, Komatsu T, Takamizo T, Fujimori M (2006) Development of simple sequence repeat (SSR) markers and construction of an SSR-based linkage map in Italian ryegrass (Lolium multiflorum Lam.). Theor Appl Genet 113:270–279
Hohmann S, Kadereit J, Kadereit G (2006) Understanding Mediterranean-Californian disjunctions: molecular evidence from Chenopodiaceae-Betoideae. Taxon 55:67–78
Holton T, Christopher J, McClure L, Harker N, Henry R (2002) Identification and mapping of polymorphic SSR markers from expressed gene sequences of barley and wheat. Mol Breed 9:63–71
Kantety R, La Rota M, Matthews D, Sorrells M (2002) Data mining for simple sequence repeats in expressed sequence tags from barley, maize, rice, sorghum and wheat. Plant Mol Biol 48:501–510
Kosambi D (1944) The estimation of map distance from recombination values. Ann Eugen 12:172–175
Lawson M, Zhang L (2006) Distinct patterns of SSR distribution in the Arabidopsis thaliana and rice genomes. Genome Biol 7:R14
Liewlaksaneeyanawin C, Ritland C, El-Kassaby Y, Ritland K (2004) Single-copy, species-transferable microsatellite markers developed from loblolly pine ESTs. Theor Appl Genet 109:361–369
Mielordt S (2005) Gene prediction in Arabidopsis thaliana. Master thesis in bioinformatics, FU Berlin (2005)
Milbourne D, Meyer R, Collins A, Ramsay I, Gebhardt C, Waugh R (1998) Isolation, characterization and mapping of simple sequence repeat loci in potato. Mol Gen Genet 259:233–245
McGrath JM, Trebbi D, Fenwick A, Panella L, Schultz B, Laurent V, Barnes S, Murray S (2007) An open-source first-generation molecular genetic map from a sugar × table beet cross and its extension to physical mapping. Plant Genome, a Supp to Crop Sci 47:S49–S66
Metzgar D, Bytof J, Wills C (2000) Selection against frameshift mutations limits microstellite expansion in coding DNA. Genome Res 10:72–80
Monfort A, Vilanova S, Davis T, Arus P (2006) A new set of polymorphic simple sequence repeat (SSR) markers from a wild strawberry (Fragaria vesca) are transferable to other diploid Fragaria species and to Fragaria × ananassa. Mol Ecol Note 6:197–200
Monforte A (2003) Development and mapping of SSR markers from melon ESTs. 7th international congress on plant molecular biology. ISPMB 2003, Barcelona, 23–28 June
Mörchen M, Cuguen J, Michaelis G, Hänni C, Saumitou-Laprade P (1996) Abundance and length polymorphism of microsatellite repeat in Beta vulgaris L. Theor Appl Genet 92:326–333
Morgante M, Hanafey M, Powell W (2002) Microsatellites are preferentially associated with nonrepetitive DNA in plant genomes. Nat Genet 30:194–200
Nilsson N, Halldén C, Hansen M, Hjerdin A, Säll T (1997) Comparing the distribution of RAPD and RFLP markers in a high density linkage map of sugar beet. Genome 40:644–651
Nilsson N, Hansen M, Panagopoulos A, Tuvesson S, Ehlde M, Christiansson M, Rading I, Rissler M, Kraft T (1999) QTL analysis of Cercospora leaf spot resistance in sugar beet. Plant Breed 118:327–334
Pelsy F, Merdinoglu D (1996) Identification and mapping of random amplified polymorphic DNA markers linked to a rhizomania resistance gene in sugar beet (Beta vulgaris L.) by bulked segregant analysis. Plant Breed 115:371–377
Pillen K, Steinrücken G, Wricke G, Herrmann R, Jung C (1992) A linkage map of sugar beet (Beta vulgaris L.). Theor Appl Genet 84:129–135
Qureshi S, Saha S, Kantety R, Jenkins J (2004) EST-SSR: a new class of genetic markers in cotton. J Cotton Sci 8:112–123
Rae S, Aldam C, Domingez I, Hoebrechts M, Barnes S, Edwards K (2000) Development and incorporation of microsatellite markers into the linkage map of sugar beet (Beta vulgaris L.). Theor Appl Genet 100:1240–1248
Richards C, Brownson M, Mitchell S, Kresovich S, Panella L (2004) Polymorphic microsatellite markers for inferring diversity in wild and domesticated sugar beet (Beta vulgaris). Mol Ecol Notes 4:243
Röder M, Plaschke J, König S, Börner A, Sorrells M, Tanksley S, Ganal M (1995) Abundance, variability and chromosomal location of microsatellites in wheat. Mol Gen Genet 246:327–333
Roundy T, Theurer J (1974) Linkage and inheritance studies involving an annual pollen restorer and other genetic characters in sugar beets. Crop Sci 14:230–232
Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386
Rudd S, Mewes H, Mayer K (2003) SPUTNIK: a database platform for comparative plant genomics. Nucleic Acids Res 31:128–132
Saha M, Mian M, Eujayl I, Zwonitzer J, Wang L, May G (2004) Tall fescue EST-SSR markers with transferability across several grass species. Theor Appl Genet 109:783–791
Santoni S, Bervillé A (1992) Two different satellite DNAs in Beta vulgaris L.: evolution, quantification and distribution in the genus. Theor Appl Genet 84:1009–1016
Schäfer-Pregl R, Borchardt D, Barzen E, Glass C, Mechelke W, Seitzer J, Salamini F (1999) Localization of QTLs for tolerance to Cercospora beticola on sugar beet linkage groups. Theor Appl Genet 99:829–836
Schmidt T, Heslop-Harrison J (1996) The physical and genomic organization of microsatellites in sugar beet. Proc Natl Acad Sci USA 93:8761–8765
Schneider K, Borchardt D, Schäfer-Pregl R, Nagl N, Glass C, Jeppsson A, Gebhardt C, Salamini F (1999) PCR-based cloning and segregation analysis of functional gene homologues in Beta vulgaris. Mol Gen Genet 262:515–524
Schneider K, Schäfer-Pregl R, Borchardt D, Salamini F (2002) Mapping QTLs for sucrose content, yield and quality in a sugar beet population fingerprinted by EST-related markers. Theor Appl Genet 104:1107–1113
Scholten O, Klein-Lankhorst R, Esselink D, De Bock T, Lange W (1997) Identification and mapping of random amplified polymorphic DNA (RAPD) markers linked to resistance against beet necrotic yellow vein virus (BNYVV) in Beta accessions. Theor Appl Genet 94:123–130
Schondelmaier J, Steinrücken G, Jung C (1996) Integration of AFLP markers into a linkage map of sugar beet (Beta vulgaris L.). Plant Breed 115:231–237
Schondelmaier J, Jung C (1997) Chromosomal assignment of the nine linkage groups of sugar beet (Beta vulgaris L.) using primary trisomics. Theor Appl Genet 95:590–596
Schumacher K, Schondelmaier J, Barzen E, Steinrücken G, Borchardt D, Weber W, Jung C, Salamini F (1997) Combining different linkage maps in sugar beet (Beta vulgaris L.) to make one map. Plant Breed 116:23–38
Sorrells M (2000) The evolution of comparative plant genetics. In: Gustafson JP (ed) Genomes. Proceedings of 22nd stadler symposium (6–8 june 1998, Columbia). Kluwer academic publishers, Boston
Temnykh S, DeClerck G, Lukashova A, Lipovich L, Cartinhour S, McCouch S (2001) Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. Genome Res 11:1441–1452
Thiel T, Michalek W, Varshney R, Graner A (2003) Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor Appl Genet 106:411–422
Uphoff H, Wricke G (1995) A genetic map of sugar beet (Beta vulgaris) based on RAPD markers. Plant Breed 114:355–357
Van Ooijen J, Voorrips R (2001) Joinmap® 3.0, Software for the calculation of genetics linkage maps. Plant Research International, Wageningen
Viard F, Bernard J, Desplanque B (2002) Crop–weed interactions in the Beta vulgaris complex at a local scale: allelic diversity and gene flow within sugar beet fields. Theor Appl Genet 104:688–697
Viard F, Arnaud JF, Delescluse M, Cuguen J (2004) Tracing back seed and pollen flow within the crop–wild Beta vulgaris complex: genetic distinctiveness vs. hot spots of hybridization over a regional scale. Mol Ecol 13:1357–1364
Wagner H, Weber W, Wricke G (1992) Estimating linkage relationship of isozyme markers and morphological markers in sugar beet (Beta vulgaris L.) including families with distorted segregations. Plant Breed 108:89–96
Weber W, Borchardt D, Koch G (1999) Combined linkage maps and QTLs in sugar beet (Beta vulgaris L.) from different populations. Plant Breed 118:193–204
Weber W, Borchardt D, Koch G (2000) Markers analysis for quantitative traits in sugar beet. Plant Breed 119:97–106
Zane L, Bargelloni L, Patarnello T (2002) Strategies for microsatellite isolation: a review. Mol Ecol 11:1–16
Zhang L, Bernard M, Leroy P, Feuillet C, Sourdille P (2005) High transferability of bread wheat EST-derived SSRs to other cereals. Theor Appl Genet 111:677–687
Acknowledgments
We thank K. Bounan for crossing and growing the plants, B. Devaux for primary selection of EST-SSRs on parents and its F1 and S Barnes and JF Arnaud for useful discussions. We are grateful to M. McGrath for the numerous exchanges during map construction and assignation to chromosomes. We thank Ets Florimond Desprez and the German Federal Ministry for Education and Research (BMBF Grant No 0312706A) for Financial support.
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Communicated by A. Kilian.
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Laurent, V., Devaux, P., Thiel, T. et al. Comparative effectiveness of sugar beet microsatellite markers isolated from genomic libraries and GenBank ESTs to map the sugar beet genome. Theor Appl Genet 115, 793–805 (2007). https://doi.org/10.1007/s00122-007-0609-y
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DOI: https://doi.org/10.1007/s00122-007-0609-y