Skip to main content
Log in

Evolution of chromosome 6 of Solanum species revealed by comparative fluorescence in situ hybridization mapping

  • RESEARCH ARTICLE
  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

Comparative genetic linkage mapping using a common set of DNA markers in related species is an important methodology in plant genome research. Here, we demonstrate a comparative fluorescence in situ hybridization (FISH) mapping strategy in plants. A set of 13 bacterial artificial chromosome clones spanning the entire length of potato chromosome 6 was used for pachytene chromosome-based FISH mapping in seven distantly related Solanum species including potato, tomato, and eggplant. We discovered one paracentric inversion and one pericentric inversion within specific lineages of these species. The comparative FISH mapping data revealed the ancestral structure of this chromosome. We demonstrate that comparative FISH mapping is an efficient and powerful methodology to study chromosomal evolution among plant species diverged for up to 12 million years.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Amarillo FIE, Bass HW (2007) A transgenomic cytogenetic sorghum (Sorghum propinquum) bacterial artificial chromosome fluorescence in situ hybridization map of maize (Zea mays L.) pachytene chromosome 9, evidence for regions of genome hyperexpansion. Genetics 177:1509–1526

    Article  PubMed  CAS  Google Scholar 

  • Barton DW (1950) Pachytene morphology of the tomato chromosome complement. Am J Bot 37:639–643

    Article  Google Scholar 

  • Cheng ZK, Presting GG, Buell CR, Wing RA, Jiang JM (2001) High-resolution pachytene chromosome mapping of bacterial artificial chromosomes anchored by genetic markers reveals the centromere location and the distribution of genetic recombination along chromosome 10 of rice. Genetics 157:1749–1757

    CAS  PubMed  Google Scholar 

  • D'Arcy WG (1972) Solanaceae studies II: typication of subdivisions of Solanum. Ann Missouri Bot Gard 59:262–278

    Article  Google Scholar 

  • Debener T, Salamini F, Gebhardt C (1990) Phylogeny of wild and cultivated Solanum species based on nuclear restriction fragment length polymorphisms (RFLPs). Theor Appl Genet 79:360–368

    Article  CAS  Google Scholar 

  • Devos KM, Gale MD (2000) Genome relationships: the grass model in current research. Plant Cell 12:637–646

    Article  CAS  PubMed  Google Scholar 

  • Doganlar S, Frary A, Daunay MC, Lester RN, Tanksley SD (2002) 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 

  • Dong F, Song J, Naess SK, Helgeson JP, Gebhardt C, Jiang J (2000) Development and applications of a set of chromosome-specific cytogenetic DNA markers in potato. Theor Appl Genet 101:1001–1007

    Article  CAS  Google Scholar 

  • Eder V, Ventura M, Ianigro M, Teti M, Rocchi M, Archidiacono N (2003) Chromosome 6 phylogeny in primates and centromere repositioning. Mol Biol Evol 20:1506–1512

    Article  CAS  PubMed  Google Scholar 

  • Fransz PF, Alonso-Blanco C, Liharska TB, Peeters AJM, Zabel P, de Jong JH (1996) High-resolution physical mapping in Arabidopsis thaliana and tomato by fluorescence in situ hybridization to extended DNA fibres. Plant J 9:421–430

    Article  CAS  PubMed  Google Scholar 

  • Han YH, Zhang ZH, Liu CX, Liu JH, Huang SW, Jiang JM, Jin WW (2009) Centromere repositioning in cucurbit species: implication of the genomic impact from centromere activation and inactivation. Proc Nat Acad Sci USA 106:14937–14941

    Article  CAS  PubMed  Google Scholar 

  • Howell EC, Armstrong SJ, Barker GC, Jones GH, King GJ, Ryder CD, Kearsey MJ (2005) Physical organization of the major duplication on Brassica oleracea chromosome O6 revealed through fluorescence in situ hybridization with Arabidopsis and Brassica BAC probes. Genome 48:1093–1103

    Article  CAS  PubMed  Google Scholar 

  • Iovene M, Wielgus SM, Simon PW, Buell CR, Jiang JM (2008) Chromatin structure and physical mapping of chromosome 6 of potato and comparative analyses with tomato. Genetics 180:1307–1317

    Article  CAS  PubMed  Google Scholar 

  • Jackson SA, Wang ML, Goodman HM, Jiang JM (1998) Application of fiber-FISH in physical mapping of Arabidopsis thaliana. Genome 41:566–572

    Article  CAS  PubMed  Google Scholar 

  • Jackson SA, Cheng ZK, Wang ML, Goodman HM, Jiang J (2000) Comparative fluorescence in situ hybridization mapping of a 431-kb Arabidopsis thaliana bacterial artificial chromosome contig reveals the role of chromosomal duplications in the expansion of the Brassica rapa genome. Genetics 156:833–838

    CAS  PubMed  Google Scholar 

  • Jiang JM, Gill BS (2006) Current status and the future of fluorescence in situ hybridization (FISH) in plant genome research. Genome 49:1057–1068

    Article  CAS  PubMed  Google Scholar 

  • Jiang JM, Gill BS, Wang GL, Ronald PC, Ward DC (1995) Metaphase and interphase fluorescence in situ hybridization mapping of the rice genome with bacterial artificial chromosomes. Proc Natl Acad Sci USA 92:4487–4491

    Article  CAS  PubMed  Google Scholar 

  • Knapp S, Bohs L, Nee M, Spooner DM (2004) Solanaceae—a model for linking genomics with biodiversity. Comp Funct Genom 5:285–291

    Article  CAS  Google Scholar 

  • Koo DH, Jiang JM (2009) Super-stretched pachytene chromosomes for fluorescence in situ hybridization mapping and immunodetection of DNA methylation. Plant J 59:509–516

    Article  CAS  PubMed  Google Scholar 

  • Koumbaris GL, Bass HW (2003) A new single-locus cytogenetic mapping system for maize (Zea mays L.): overcoming FISH detection limits with marker-selected sorghum (S. propinquum L.) BAC clones. Plant J 35:647–659

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Lysak MA, Fransz PF, Ali HBM, Schubert I (2001) Chromosome painting in Arabidopsis thaliana. Plant J 28:689–697

    Article  CAS  PubMed  Google Scholar 

  • Lysak MA, Berr A, Pecinka A, Schmidt R, McBreen K, Schubert I (2006) Mechanisms of chromosome number reduction in Arabidopsis thaliana and related Brassicaceae species. Proc Natl Acad Sci USA 103:5224–5229

    Article  CAS  PubMed  Google Scholar 

  • Matsubayashi M (1991) Phylogenetic relationships in the potato and its related species. In: Tsuchiya T, Gupta P (eds) Chromosome engineering in plants: genetics, breeding, evolution. Elsevier, Amsterdam, pp 93–118

    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

    CAS  PubMed  Google Scholar 

  • Olmstead RG, Bohs L (2006) A summary of molecular systematic research in the Solanaceae: 1982–2006. Acta Hort 745:255–268

    Google Scholar 

  • Perez F, Menendez A, Dehal P, Quiros CF (1999) Genomic structural differentiation in Solanum: comparative mapping of the A- and E-genomes. Theor Appl Genet 98:1183–1193

    Article  CAS  Google Scholar 

  • Rodriguez F, Spooner DM (2009) Nitrate reductase phylogeny of potato (Solanum sect. Petota) genomes with emphasis on the origins of the polyploid species. Syst Bot 34:207–219

    Article  Google Scholar 

  • Spooner DM, Castillo R (1997) Reexamination of series relationships of South American wild potatoes (Solanaceae: Solanum sect Petota): evidence from chloroplast DNA restriction site variation. Am J Bot 84:671–685

    Article  CAS  Google Scholar 

  • Spooner DM, Anderson GJ, Jansen RK (1993) Chloroplast DNA evidence for the interrelationships of tomatoes, potatoes, and pepinos (Solanaceae). Am J Bot 80:676–688

    Article  CAS  Google Scholar 

  • Tang XM, Szinay D, Lang C, Ramanna MS, van der Vossen EAG, Datema E, Lankhorst RK, de Boer J, Peters SA, Bachem C, Stiekema W, Visser RGF, de Jong H, Bai YL (2008) Cross-species bacterial artificial chromosome-fluorescence in situ hybridization painting of the tomato and potato chromosome 6 reveals undescribed chromosomal rearrangements. Genetics 180:1319–1328

    Article  CAS  PubMed  Google Scholar 

  • Tanksley SD, Ganal MW, Prince JP, de Vicente MC, Bonierbale MW, Broun P, Fulton TM, Giovannoni JJ, Grandillo S, Martin GB, Messeguer R, Miller JC, Miller L, Paterson AH, Pineda O, Roder MS, Wing RA, Wu W, Young ND (1992) High-density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160

    CAS  PubMed  Google Scholar 

  • Valarik M, Bartos J, Kovarova P, Kubalakova M, de Jong JH, Dolezel J (2004) High-resolution FISH on super-stretched flow-sorted plant chromosomes. Plant J 37:940–950

    Article  CAS  PubMed  Google Scholar 

  • Wienberg J, Stanyon R (1997) Comparative painting of mammalian chromosomes. Curr Opin Genet Dev 7:784–791

    Article  CAS  PubMed  Google Scholar 

  • Wikstrom N, Savolainen V, Chase MW (2001) Evolution of the angiosperms: calibrating the family tree. Proc R Soc Lond B Biol Sci 268:2211–2220

    Article  CAS  Google Scholar 

  • Wu FN, Eannetta NT, Xu YM, Tanksley SD (2009) 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 

  • Yeh BP, Peloquin SJ (1965) Pachytene chromosomes of the potato (Solanum tuberosum, group Andigena). Am J Bot 52:1014–1020

    Article  Google Scholar 

  • Ziolkowski PA, Sadowski J (2002) FISH-mapping of rDNAs and Arabidopsis BACs on pachytene complements of selected Brassicas. Genome 45:189–197

    Article  CAS  PubMed  Google Scholar 

  • Zwick MS, Hanson RE, McKnight TD, IslamFaridi MN, Stelly DM, Wing RA, Price HJ (1997) A rapid procedure for the isolation of C 0 t-1 DNA from plants. Genome 40:138–142

    Article  CAS  PubMed  Google Scholar 

  • Zwick MS, Islam-Faridi MN, Czeschin DG Jr, Wing RA, Hart GE, Stelly DM, Price HJ (1998) Physical mapping of the liguleless linkage group in Sorghum bicolor using rice RFLP-selected sorghum BACs. Genetics 148:1983–1992

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grant DBI-0604907 from the National Science Foundation. Q.F.L. was supported by a fellowship from the Ministry of Education, the People’s Republic of China. D.M.S. was supported by the USDA and by NSF DEB 0316614 and USDA National Research Initiative Grant 2008-35300-18669. M.I. was on leave of absence from CNR—Institute of Plant Genetics, Via Amendola 165/A, 70126 Bari, Italy.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jiming Jiang.

Additional information

Communicated by P. Shaw

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lou, Q., Iovene, M., Spooner, D.M. et al. Evolution of chromosome 6 of Solanum species revealed by comparative fluorescence in situ hybridization mapping. Chromosoma 119, 435–442 (2010). https://doi.org/10.1007/s00412-010-0269-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00412-010-0269-6

Keywords

Navigation