Skip to main content
SpringerLink
Log in

EST, COSII, and arbitrary gene markers give similar estimates of nucleotide diversity in cultivated tomato (Solanum lycopersicum L.)

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Because cultivated tomato (Solanum lycopersicum L.) is low in genetic diversity, public, verified single nucleotide polymorphism (SNP) markers within the species are in demand. To promote marker development we resequenced approximately 23 kb in a diverse set of 31 tomato lines including TA496. Three classes of markers were sampled: (1) 26 expressed-sequence tag (EST), all of which were predicted to be polymorphic based on TA496, (2) 14 conserved ortholog set II (COSII) or unigene, and (3) ten published sequences, composed of nine fruit quality genes and one anonymous RFLP marker. The latter two types contained mostly noncoding DNA. In total, 154 SNPs and 34 indels were observed. The distributions of nucleotide diversity estimates among marker types were not significantly different from each other. Ascertainment bias of SNPs was evaluated for the EST markers. Despite the fact that the EST markers were developed using SNP prediction within a sample consisting of only one TA496 allele and one additional allele, the majority of polymorphisms in the 26 EST markers were represented among the other 30 tomato lines. Fifteen EST markers with published SNPs were more closely examined for bias. Mean SNP diversity observations were not significantly different between the original discovery sample of two lines (53 SNPs) and the 31 line diversity panel (56 SNPs). Furthermore, TA496 shared its haplotype with at least one other line at 11 of the 15 markers. These data demonstrate that public EST databases and noncoding regions are a valuable source of unbiased SNP markers in tomato.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Andolfatto P (2001) Adaptive hitchhiking effects on genome variability. Curr Opin Genet Dev 11:635–641

    Article  PubMed  CAS  Google Scholar 

  • Aracri B, Bartley GE, Scolnik PA, Giuliano G (1994) Sequence of the phytoene desaturase locus of tomato. Plant Physiol 106:789

    Article  PubMed  CAS  Google Scholar 

  • Baldo AM, Lamboy WF, Robertson LD, Sheffer SM, Labate JA (2007) The distribution of genetic variation in cultivated tomato. P170. Plant and Animal Genome XV, San Diego

    Google Scholar 

  • Brumfield RT, Beerli P, Nickerson DA, Edwards SV (2003) The utility of single nucleotide polymorphisms in inferences of population history. Trends Ecol Evol 18:249–256

    Article  Google Scholar 

  • Charlesworth D (2003) Effects of inbreeding on the genetic diversity of populations. Philos Trans R Soc Lond Ser B 358:1051–1070

    Article  CAS  Google Scholar 

  • Chikhi L (2008) Genetic markers: how accurate can genetic data be? Heredity 101(6):471–472. doi:10.1038/hdy.2008.106

    Article  PubMed  CAS  Google Scholar 

  • Clark AG, Hubisz MJ, Bustamente CD, Williamson SH, Nielsen R (2005) Ascertainment bias in studies of human genome-wide polymorphism. Genome Res 15:1496–1502

    Article  PubMed  CAS  Google Scholar 

  • Cogan N, Drayton M, Ponting R, Vecchies A, Bannan N, Sawbridge T, Smith K, Spangenberg G, Forster J (2007) Validation of in silico-predicted genic SNPs in white clover (Trifolium repens L.), an outbreeding allopolyploid species. Mol Genet Genom 277:413–425

    Article  CAS  Google Scholar 

  • Colosi JC, Schaal B (1993) Tissue grinding with ball bearing and vortex mixer for DNA extraction. Nucleic Acids Res 21:1051–1052

    Article  PubMed  CAS  Google Scholar 

  • Crouzillat D, Wu F, Rigoreau M, Lin C, Mueller L, Tanksley S, Petiard V (2006) A synteny map for coffee based on COSII markers. Abstract 51. Solanaceae 2006, Madison

  • Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8:186–194

    PubMed  CAS  Google Scholar 

  • Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8:175–185

    PubMed  CAS  Google Scholar 

  • Foolad MR (2007) Genome mapping and molecular breeding of tomato. Int J Plant Genomics 2007. doi:10.1155/2007/64358

  • Francis D, Yang W, van der Knaap E, Hogenhout S, Deynze AV, Darrigues A (2006) DNA-microarray detection of single feature polymorphisms as a discovery tool for marker assisted selection within elite tomato populations. W299. Plant and Animal Genome XIV, San Diego

    Google Scholar 

  • Fukuoka H, Miyatake K, Nunome T, Ohyama A, Negoro S, Kono I, Kanamori H, Yamaguchi H (2007) EST sequencing in eggplant and comparative sequence analysis for DNA marker development in Solanum species. P4. Plant and Animal Genome XV, San Diego

    Google Scholar 

  • Fulton T, Van der Hoeven R, Eannetta N, Tanksley S (2002) Identification, analysis, and utilization of conserved ortholog set markers for comparative genomics in higher plants. Plant Cell 14:1457–1467

    Article  PubMed  CAS  Google Scholar 

  • Ganal MW, Durstewitz G, Kulosa D, Luerssen H, Polley A, Wolf M (2007) Development of EST-derived SNP markers for plant breeding. W172. Plant and Animal Genome XV, San Diego

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hayes B, Laerdahl JK, Lien S, Moen T, Berg P, Hindar K, Davidson WS, Koop BF, Adzhubei A, Hoyheim B (2007) An extensive resource of single nucleotide polymorphism markers associated with Atlantic salmon (Salmo salar) expressed sequences. Aquaculture 265:82–90

    Article  CAS  Google Scholar 

  • Hirschberg J, Ronen G, Zamir D (2001) Tomato gene B polynucleotides coding for lycopene cyclase. Patent number US 6252141

  • Isaacson T, Ronen G, Zamir D, Hirschberg J (2002) Cloning of tangerine from tomato reveals a carotenoid isomerase essential for the production of beta-carotene and xanthophylls in plants. Plant Cell 14:333–342

    Article  PubMed  CAS  Google Scholar 

  • Iseli C, Jongeneel CV, Bucher P (1999) ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proc Int Conf Intell Syst Mol Biol, pp 138–148

  • Jones E, Sullivan H, Bhattramakki D, Smith J (2007) A comparison of simple sequence repeat and single nucleotide polymorphism marker technologies for the genotypic analysis of maize (Zea mays L.). Theor Appl Genet 115:361–371

    Article  PubMed  CAS  Google Scholar 

  • Jorde LB, Watkins WS, Bamshad MJ, Dixon ME, Ricker CE, Seielstad MT, Batzer MA (2000) The distribution of human genetic diversity: a comparison of mitochondrial, autosomal, and Y-chromosome data. Am J Hum Genet 66:979–988

    Article  PubMed  CAS  Google Scholar 

  • Josse E-M, Simkin AJ, Gaffe J, Labouré A-M, Kuntz M, Carol P (2000) A plastid terminal oxidase associated with carotenoid desaturation during chromoplast differentiation. Plant Physiol 123:1427–1436

    Article  PubMed  CAS  Google Scholar 

  • Labate JA, Baldo AM (2005) Tomato SNP discovery by EST mining and resequencing. Mol Breed 16:343–349

    Article  CAS  Google Scholar 

  • Labate JA, Robertson LD, Sheffer SM, Lamboy WF, Baldo AM (2006) EST-based SNP markers: is there ascertainment bias in tomato? Annual meeting of the society for the study of evolution, Stony Brook

  • Labate JA, Grandillo S, Fulton T, Muños S, Caicedo AL, Peralta I et al (2007) Tomato. In: Kole C (ed) Genome mapping and molecular breeding in plants: vegetables. Springer, New York, pp 1–125

    Google Scholar 

  • Lottaz C, Iseli C, Jongeneel C, Bucher P (2003) Modeling sequencing errors by combining Hidden Markov models. Bioinformatics 19:103–112

    Article  Google Scholar 

  • Luerssen H, Polley A, Ganal M (2006) SNP identification in tomato and pepper using comparative sequencing. W178. Plant and Animal Genome XIV, San Diego

    Google Scholar 

  • Miller JC, Tanksley SD (1990) RFLP analysis of phylogenetic relationships and genetic variation in the genus Lycopersicon. Theor Appl Genet 80:437–448

    CAS  Google Scholar 

  • Moncada P, Montoya JC, Lopez G, Gonzalez A, Iriarte G, Zarate LA, Cristancho M (2006) Advances in construction of tetraploid and diploid maps and in populations for QTL analysis in coffee. Abstract 56. Solanaceae 2006, Madison

  • Monforte AJ, Friedman E, Zamir D, Tanksley SD (2001) Comparison of a set of allelic QTL-NILs for chromosome 4 of tomato: deductions about natural variation and implications for germplasm utilization. Theor Appl Genet 102:572–590

    Article  CAS  Google Scholar 

  • Mustilli AC, Fenzi F, Ciliento R, Alfano F, Bowler C (1999) Phenotype of the tomato high pigment-2 mutant is caused by a mutation in the tomato homolog of DEETIOLATED1. Plant Cell 11:145–157

    Article  PubMed  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nesbitt TC, Tanksley SD (2002) Comparative sequencing in the genus Lycopersicon: implications for the evolution of fruit size in the domestication of cultivated tomatoes. Genetics 162:365–379

    PubMed  CAS  Google Scholar 

  • Olarte A, Barrero LS, Lobo M, Tanksley S (2006) Use of COS markers for the Andean fruited species lulo and tree tomato. Abstract 385. Solanaceae 2006, Madison

  • Park YH, West MAL, St Clair DA (2004) Evaluation of AFLPs for germplasm fingerprinting and assessment of genetic diversity in cultivars of tomato (Lycopersicon esculentum L.). Genome 47:510–518

    Article  PubMed  CAS  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Pritchard JK (2001) Deconstructing maize population structure. Nat Genet 28:203–204

    Article  PubMed  CAS  Google Scholar 

  • Ray J, Moreau P, Bird C, Bird A, Grierson D, Maunders M, Truesdale M, Bramley P, Schuch W (1992) Cloning and characterization of a gene involved in phytoene synthesis from tomato. Plant Mol Biol 19:401–404

    Article  PubMed  CAS  Google Scholar 

  • Rick CM, Laterrot H, Philouze J (1990) A revised key for the Lycopersicon species. Tomato Genet Coop Rep 40:31

    Google Scholar 

  • Robbins MD, Yang W, van der Knaap E, Francis D (2007) SNP variation and patterns of selection in lineages of cultivated tomato. P172. Plant and Animal Genome XV, San Diego

    Google Scholar 

  • Rodriguez F, Wu F, Tanksley S, Spooner D (2006) A multiple single-copy gene phylogenetic analysis of wild tomatoes (Solanum L. section Lycopersicon (Mill.) Wettst.) and their outgroup relatives. Abstract 193. Solanaceae 2006, Madison

  • Ronen G, Carmel-Goren L, Zamir D, Hirschberg J (2000) An alternative pathway to beta-carotene formation in plant chromoplasts discovered by map-based cloning of beta and old-gold color mutations in tomato. Proc Natl Acad Sci USA 97:11102–11107

    Article  PubMed  CAS  Google Scholar 

  • Roselius K, Stephan W, Stadler T (2005) The relationship of nucleotide polymorphism, recombination rate and selection in wild tomato species. Genetics 171:753–763

    Article  PubMed  CAS  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Saliba-Colombani V, Causse M, Gervais L, Philouze J (2000) Efficiency of RFLP, RAPD, and AFLP markers for the construction of an intraspecific map of the tomato genome. Genome 43:29–40

    Article  PubMed  CAS  Google Scholar 

  • Schlötterer C, Harr B (2002) Single nucleotide polymorphisms derived from ancestral populations show no evidence for biased diversity estimates in Drosophila melanogaster. Mol Ecol 11:947–950

    Article  PubMed  Google Scholar 

  • Sim S-C, Yang W, van der Knaap E, Hogenhout S, Xiao H, Francis D (2007) Microarray-based SNP discovery for tomato genetics and breeding. P173. Plant and Animal Genome XV, San Diego

    Google Scholar 

  • Smith CT, Antonovich A, Templin WD, Elfstrom CM, Narum SR, Seeb LW (2007) Impacts of marker class bias relative to locus-specific variability on population inferences in chinook salmon: a comparison of single-nucleotide polymorphisms with short tandem repeats and allozymes. Trans Am Fish Soc 136:1674–1687

    Article  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry: the principles and practice of statistics in biological research, 2nd edn. Freeman, New York

    Google Scholar 

  • SolCAP (2008) USDA-CSREES awards $5.4 million to SolCAP. In: Zarka K (ed) SolCAP Newsl. Michigan State University, East Lansing, 5pp

    Google Scholar 

  • Stephens M, Donnelly P (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162–1169

    Article  PubMed  CAS  Google Scholar 

  • Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    Article  PubMed  CAS  Google Scholar 

  • Stevens M, Rick C (1986) Genetics and breeding. In: Atherton J, Rudich J (eds) The tomato crop. Chapman and Hall, NY, pp 35–109

    Google Scholar 

  • Tanksley SD, Grandillo S, Fulton TM, Zamir D, Eshed Y, Petiard V, Lopez J, Beck-Bunn T (1996) Advanced backcross QTL analysis in a cross between an elite processing line of tomato and its wild relative L. pimpinellifolium. Theor Appl Genet 92:213–224

    Article  CAS  Google Scholar 

  • Tanksley SD, Bernachi D, Beck-Bunn Teresa, Emmatty D, Eshed Y, Inai S, Lopez J, Petiard V, Sayama H, Uhlig J, Zamir D (1998) Yield and quality evaluations on a pair of processing tomato lines nearly isogenic for the Tm-2 a gene for resistance to the tobacco mosaic virus. Euphytica 99:77–83

    Article  Google Scholar 

  • Usuka J, Brendel V (2000) Gene structure prediction by spliced alignment of genomic DNA with protein sequences: increased accuracy by differential splice site scoring. J Mol Biol 297:1075–1085

    Article  PubMed  CAS  Google Scholar 

  • Usuka J, Zhu W, Brendel V (2000) Optimal spliced alignment of homologous cDNA to a genomic DNA template. Bioinformatics 16:203–211

    Article  PubMed  CAS  Google Scholar 

  • Van Deynze A, Stoffel K, Buell CR, Kozik A, Liu J, van der Knaap E, Francis D (2007) Diversity in conserved genes in tomato. BMC Genom 8:465

    Article  Google Scholar 

  • Villand J, Skroch PW, Lai T, Hanson P, Kuo CG, Nienhuis J (1998) Genetic variation among tomato accessions from primary and secondary centers of diversity. Crop Sci 38:1339–1347

    Article  Google Scholar 

  • Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J (2002) A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (Rin) locus. Science 296:343–346

    Article  PubMed  CAS  Google Scholar 

  • Wu F, Mueller LA, Crouzillat D, Petiard V, Tanksley SD (2006) Combining bioinformatics and phylogenetics to identify large sets of single-copy orthologous genes (COSII) for comparative, evolutionary and systematic studies: a test case in the Euasterid plant clade. Genetics 174:1407–1420

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto N, Tsugane T, Watanabe M, Yano K, Maeda F, Kuwata C, Torki M, Ban Y, Nishimura S, Shibata D (2005) Expressed sequence tags from the laboratory-grown miniature tomato (Lycopersicon esculentum) cultivar Micro-Tom and mining for single nucleotide polymorphisms and insertions/deletions in tomato cultivars. Gene 356:127–134

    Article  PubMed  Google Scholar 

  • Yang WC, Bai XD, Kabelka E, Eaton C, Kamoun S, van der Knaap E, Francis D (2004) Discovery of single nucleotide polymorphisms in Lycopersicon esculentum by computer aided analysis of expressed sequence tags. Mol Breed 14:21–34

    Article  CAS  Google Scholar 

  • Yang L, Jin G, Zhao X, Zheng Y, Xu Z, Wu W (2007) PIP: a database of potential intron polymorphism markers. Bioinformatics. doi:10.1093/bioinformatics/btm1296

  • Yates HE, Frary A, Doganlar S, Frampton A, Eannetta NT, Uhlig J, Tanksley SD (2004) Comparative fine mapping of fruit quality QTLs on chromosome 4 introgressions derived from two wild tomato species. Euphytica 135:283–296

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank S. Sheffer, W. Lamboy, P. Kisly, T. Balch, and K. Timmer for excellent technical assistance. Dr. D. Spooner provided unpublished data for COSII markers, and Dr. J. Giovannoni provided primer sequences for rin. This work was funded by CRIS project 1907-21000-006-00D

Author information

Authors and Affiliations

  1. USDA-ARS Plant Genetic Resources Unit, 630 W. North Street, Geneva, NY, 14456, USA

    Joanne A. Labate, Larry D. Robertson & Angela M. Baldo

  2. Department of Plant Breeding and Genetics, Cornell University, Ithaca, NY, 14853, USA

    Feinan Wu & Steven D. Tanksley

Authors
  1. Joanne A. Labate
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Larry D. Robertson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Feinan Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Steven D. Tanksley
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Angela M. Baldo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joanne A. Labate.

Additional information

Communicated by A. Schulman.

The use of trade, firm, or corporation names in this publication is for the information and convenience of the reader. Such use does not constitute an official endorsement or approval by the United States Department of Agriculture or the Agricultural Research Service of any product or service to the exclusion of others that may be suitable.

Electronic supplementary material

Below is the link to the electronic supplementary material.

File “sequences.fas.txt” contains FASTA formatted DNA sequences of all 50 markers for line TA496. Annotations are included. Alignment gaps (-) or missing (?) data relative to additional sequences were retained to preserve annotation nucleotide positions.

(TXT 27 kb)

Table S1 and Fig. S1

(PPT 156 kb)

Table S2

(DOC 34 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Labate, J.A., Robertson, L.D., Wu, F. et al. EST, COSII, and arbitrary gene markers give similar estimates of nucleotide diversity in cultivated tomato (Solanum lycopersicum L.). Theor Appl Genet 118, 1005–1014 (2009). https://doi.org/10.1007/s00122-008-0957-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-008-0957-2

Keywords

Search

Navigation