COSII genetic maps of two diploid Nicotiana species provide a detailed picture of synteny with tomato and insights into chromosome evolution in tetraploid N. tabacum

Abstract

Using single-copy conserved ortholog set (COSII) and simple sequence repeat (SSR) markers, we have constructed two genetic maps for diploid Nicotiana species, N. tomentosiformis and N. acuminata, respectively. N. acuminata is phylogenetically closer to N. sylvestris than to N. tomentosiformis, the latter two of which are thought to contribute the S-genome and T-genome, respectively, to the allotetraploid tobacco (N. tabacum L., 2n = 48). A comparison of the two maps revealed a minimum of seven inversions and one translocation subsequent to the divergence of these two diploid species. Further, comparing the diploid maps with a dense tobacco map revealed that the tobacco genome experienced chromosomal rearrangements more frequently than its diploid relatives, supporting the notion of accelerated genome evolution in allotetraploids. Mapped COSII markers permitted the investigation of Nicotiana–tomato syntenic relationships. A minimum of 3 (and up to 10) inversions and 11 reciprocal translocations differentiate the tomato genome from that of the last common ancestor of N. tomentosiformis and N. acuminata. Nevertheless, the marker/gene order is well preserved in 25 conserved syntenic segments. Molecular dating based on COSII sequences suggested that tobacco was formed 1.0MYA or later. In conclusion, these COSII and SSR markers link the cultivated tobacco map to those of wild diploid Nicotiana species and tomato, thus providing a platform for cross-reference of genetic and genomic information among them as well as other solanaceous species including potato, eggplant, pepper and the closely allied coffee (Rubiaceae). Therefore they will facilitate genetic research in the genus Nicotiana.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Bindler G, van der Hoeven R, Gunduz I, Plieske J, Ganal M, Rossi L, Gadani F, Donini P (2007) A microsatellite marker based linkage map of tobacco. Theor Appl Genet 114:341–349

    Article  CAS  PubMed  Google Scholar 

  2. Bogani P, Lio P, Intrieri MC, Buiatti M (1997) A physiological and molecular analysis of the genus Nicotiana. Mol Phylogenet Evol 7:62–70

    Article  CAS  PubMed  Google Scholar 

  3. Chaleff RS, Ray TB (1984) Herbicide-resistant mutants from tobacco cell-cultures. Science 223:1148–1151

    Article  PubMed  Google Scholar 

  4. Clarkson JJ, Lim KY, Kovarik A, Chase MW, Knapp S, Leitch AR (2005) Long-term genome diploidization in allopolyploid Nicotiana section Repandae (Solanaceae). New Phytol 168:241–252

    Article  CAS  PubMed  Google Scholar 

  5. Clemente T (2006) Nicotiana (Nicotiana tobaccum, Nicotiana benthamiana). Methods Mol Biol 343:143–154

    PubMed  Google Scholar 

  6. Dadejova M, Lim KY, Souckova-Skalicka K, Matyasek R, Grandbastien MA, Leitch A, Kovarik A (2007) Transcription activity of rRNA genes correlates with a tendency towards intergenomic homogenization in Nicotiana allotetraploids. New Phytol 174:658–668

    Article  CAS  PubMed  Google Scholar 

  7. Daniell H, Streatfield SJ, Wycoff K (2001) Medical molecular farming: production of antibodies, biopharmaceuticals and edible vaccines in plants. Trends Plant Sci 6:219–226

    Article  CAS  PubMed  Google Scholar 

  8. Doganlar S, Frary A, Daunay MC, Lester RN, Tanksley SD (2002a) A comparative genetic linkage map of eggplant (Solanum melongena) and its implications for genome evolution in the Solanaceae. Genetics 161:1697–1711

    CAS  PubMed  Google Scholar 

  9. Doganlar S, Frary A, Daunay MC, Lester RN, Tanksley SD (2002b) Conservation of gene function in the solanaceae as revealed by comparative mapping of domestication traits in eggplant. Genetics 161:1713–1726

    CAS  PubMed  Google Scholar 

  10. Doyle JJ, Flagel LE, Paterson AH, Rapp RA, Soltis DE, Soltis PS, Wendel JF (2008) Evolutionary genetics of genome merger and doubling in plants. Annu Rev Genet 42:443–461

    Article  CAS  PubMed  Google Scholar 

  11. Frary A, Xu YM, Liu JP, Mitchell S, Tedeschi E, Tanksley S (2005) Development of a set of PCR-based anchor markers encompassing the tomato genome and evaluation of their usefulness for genetics and breeding experiments. Theor Appl Genet 111:291–312

    Article  CAS  PubMed  Google Scholar 

  12. Freeling M, Lyons E, Pedersen B, Alam M, Ming R, Lisch D (2008) Many or most genes in Arabidopsis transposed after the origin of the order Brassicales. Genome Res 18:1924–1937

    Article  CAS  PubMed  Google Scholar 

  13. Fulton TM, van der Hoeven R, Eannetta NT, Tanksley SD (2002) Identification, analysis, and utilization of conserved ortholog set markers for comparative genomics in higher plants. Plant Cell 14:1457–1467

    Article  CAS  PubMed  Google Scholar 

  14. Gaeta RT, Pires JC, Iniguez-Luy F, Leon E, Osborn TC (2007) Genomic changes in resynthesized Brassica napus and their effect on gene expression and phenotype. Plant Cell 19:3403–3417

    Article  CAS  PubMed  Google Scholar 

  15. Goodin MM, Zaitlin D, Naidu RA, Lommel SA (2008) Nicotiana benthamiana: its history and future as a model for plant-pathogen interactions. Mol Plant Microbe Interact 21:1015–1026

    Article  CAS  PubMed  Google Scholar 

  16. Julio E, Verrier JL, de Borne FD (2006) Development of SCAR markers linked to three disease resistances based on AFLP within Nicotiana tabacum L. Theor Appl Genet 112:335–346

    Article  CAS  PubMed  Google Scholar 

  17. Kenton A, Parokonny AS, Gleba YY, Bennett MD (1993) Characterization of the Nicotiana tabacum L. genome by molecular cytogenetics. Mol Gen Genet 240:159–169

    Article  CAS  PubMed  Google Scholar 

  18. Kessler A, Halitschke R (2007) Specificity and complexity: the impact of herbivore-induced plant responses on arthropod community structure. Curr Opin Plant Biol 10:409–414

    Article  CAS  PubMed  Google Scholar 

  19. Kessler D, Gase K, Baldwin IT (2008) Field experiments with transformed plants reveal the sense of floral scents. Science 321:1200–1202

    Article  CAS  PubMed  Google Scholar 

  20. Knapp S, Chase MW, Clarkson JJ (2004) Nomenclatural changes and a new sectional classification in Nicotiana (Solanaceae). Taxon 53:73–82

    Article  Google Scholar 

  21. Konieczny A, Ausubel FM (1993) A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J 4:403–410

    Article  CAS  PubMed  Google Scholar 

  22. Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Google Scholar 

  23. Kovarik A, Matyasek R, Lim KY, Skalicka K, Koukalova B, Knapp S, Chase M, Leitch AR (2004) Concerted evolution of 18-5.8-26S rDNA repeats in Nicotiana allotetraploids. Biol J Linn Soc 82:615–625

    Article  Google Scholar 

  24. Kovarik A, Dadejova M, Lim YK, Chase MW, Clarkson JJ, Knapp S, Leitch AR (2008) Evolution of rDNA in Nicotiana allopolyploids: a potential link between rDNA homogenization and epigenetics. Ann Bot 101:815–823

    Article  CAS  PubMed  Google Scholar 

  25. Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  CAS  PubMed  Google Scholar 

  26. Leitch A, Lim KY, Skalicka K, Kovarik A (2006) Nuclear cytoplasmic interaction hypothesis and the role of translocations in Nicotiana allopolyploids. In: Cigna AA, Durante M (eds) Radiation risk estimates in normal and emergency situations. Springer, The Netherlands, pp 319–326

    Google Scholar 

  27. Lewis RS, Nicholson JS (2007) Aspects of the evolution of Nicotiana tabacum L. and the status of the United States Nicotiana Germplasm Collection. Genet Resour Crop Evol 54:727–740

    Article  Google Scholar 

  28. Lim KY, Matyasek R, Kovarik A, Leitch AR (2004) Genome evolution in allotetraploid Nicotiana. Biol J Linn Soc 82:599–606

    Article  Google Scholar 

  29. Lin TY, Kao YY, Lin S, Lin RF, Chen CM, Huang CH, Wang CK, Lin YZ, Chen CC (2001) A genetic linkage map of Nicotiana plumbaginifolia/Nicotiana longiflora based on RFLP and RAPD markers. Theor Appl Genet 103:905–911

    Article  CAS  Google Scholar 

  30. Livingstone KD, Lackney VK, Blauth JR, van Wijk R, Jahn MK (1999) Genome mapping in Capsicum and the evolution of genome structure in the solanaceae. Genetics 152:1183–1202

    CAS  PubMed  Google Scholar 

  31. Melayah D, Lim KY, Bonnivard E, Chalhoub B, De Borne FD, Mhiri C, Leitch A, Grandbastien M (2004) Distribution of the Tnt1 retrotransposon family in the amphidiploid tobacco (Nicotiana tabacum) and its wild Nicotiana relatives. Biol J Linn Soc 82:639–649

    Article  Google Scholar 

  32. Neff MM, Neff JD, Chory J, Pepper AE (1998) dCAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics. Plant J 14:387–392

    Article  CAS  PubMed  Google Scholar 

  33. Neff MM, Turk E, Kalishman M (2002) Web-based primer design for single nucleotide polymorphism analysis. Trends Genet 18:613–615

    Article  CAS  PubMed  Google Scholar 

  34. Nishi T, Tajima T, Noguchi S, Ajisaka H, Negishi H (2003) Identification of DNA markers of tobacco linked to bacterial wilt resistance. Theor Appl Genet 106:765–770

    CAS  PubMed  Google Scholar 

  35. Okamuro JK, Goldberg RB (1985) Tobacco single-copy DNA is highly homologous to sequences present in the genomes of its diploid progenitors. Mol Gen Genet 198:290–298

    Article  CAS  Google Scholar 

  36. Olmstead RG, Sweere JA, Spangler RE (1999) Phylogeny and provisional classification of the Solanaceae based on chloroplast DNA. In: Nee M, Symon DE, Lester RN, Jessop JP (eds) Solanaceae IV. Royal Botanic Gardens, Kew, pp 111–137

    Google Scholar 

  37. Petit M, Lim KY, Julio E, Poncet C, de Borne FD, Kovarik A, Leitch AR, Grandbastien MA, Mhiri C (2007) Differential impact of retrotransposon populations on the genome of allotetraploid tobacco (Nicotiana tabacum). Mol Gen Genom 278:1–15

    Article  CAS  Google Scholar 

  38. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  39. Ren N, Timko MP (2001) AFLP analysis of genetic polymorphism and evolutionary relationships among cultivated and wild Nicotiana species. Genome 44:559–571

    Article  CAS  PubMed  Google Scholar 

  40. Rossi L, Bindler G, Pijnenburg H, Isaac PG, Giraud-Henry I, Mahe M, Orvain C, Gadani F (2001) Potential of molecular marker analysis for variety identification in processed tobacco. Plant Var Seeds 14:89–101

    Google Scholar 

  41. Sanderson MJ (1997) A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol Biol Evol 14:1218–1231

    CAS  Google Scholar 

  42. Swofford DL (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, MA

    Google Scholar 

  43. Tanksley SD, Ganal MW, Prince JP, de Vicente MC, Bonierbale MW, Broun P, Fulton TM, Giovannoni JJ, Grandillo S, Martin GB (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160

    CAS  PubMed  Google Scholar 

  44. Wang Y, Diehl A, Wu FN, Vrebalov J, Giovannoni J, Siepel A, Tanksley SD (2008) Sequencing and comparative analysis of a conserved syntenic segment in the solanaceae. Genetics 180:391–408

    Article  CAS  PubMed  Google Scholar 

  45. Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42:225–249

    Article  CAS  PubMed  Google Scholar 

  46. Wu FN, 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  CAS  PubMed  Google Scholar 

  47. Wu FN, Eannetta NT, Xu YM, Durrett R, Mazourek M, Jahn MM, Tanksley SD (2009a) A COSII genetic map of the pepper genome provides a detailed picture of synteny with tomato and new insights into recent chromosome evolution in the genus Capsicum. Theor Appl Genet 118:1279–1293

    Article  CAS  PubMed  Google Scholar 

  48. Wu FN, Eannetta NT, Xu YM, Tanksley SD (2009b) A detailed synteny map of the eggplant genome based on conserved ortholog set II (COSII) markers. Theor Appl Genet 118:927–935

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Philip Morris International, Switzerland. We thank Xiaomin Jia, Ingrid S. Phillips, Doris Kriseleit and Katja Wendehake for technical assistance, Nick J. Van Eck for greenhouse work, and Dr. Lukas A. Mueller (Boyce Thompson Institute for Plant Research, Ithaca, NY, USA) and his bioinformatics group for hosting the maps and the marker data in Solanaceae Genomics Network (http://www.sgn.cornell.edu).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Steven D. Tanksley.

Additional information

Communicated by P. Heslop-Harrison.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLS 220 kb)

Supplementary material 2 (PPT 4,242 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Wu, F., Eannetta, N.T., Xu, Y. et al. COSII genetic maps of two diploid Nicotiana species provide a detailed picture of synteny with tomato and insights into chromosome evolution in tetraploid N. tabacum . Theor Appl Genet 120, 809–827 (2010). https://doi.org/10.1007/s00122-009-1206-z

Download citation

Keywords

  • Linkage Group
  • Simple Sequence Repeat Marker
  • Cleave Amplify Polymorphic Sequence
  • Tomato Genome
  • Syntenic Relationship