Abstract
Chromosomes often serve as one of the most important molecular aspects of studying the evolution of species. Indeed, most of the crucial mutations that led to differentiation of species during the evolution have occurred at the chromosomal level. Furthermore, the analysis of pachytene chromosomes appears to be an invaluable tool for the study of evolution due to its effectiveness in chromosome identification and precise physical gene mapping. By applying fluorescence in situ hybridization of 45S rDNA and CsCent1 probes to cucumber pachytene chromosomes, here, we demonstrate that cucumber chromosomes 1 and 2 may have evolved from fusions of ancestral karyotype with chromosome number n = 12. This conclusion is further supported by the centromeric sequence similarity between cucumber and melon, which suggests that these sequences evolved from a common ancestor. It may be after or during speciation that these sequences were specifically amplified, after which they diverged and specific sequence variants were homogenized. Additionally, a structural change on the centromeric region of cucumber chromosome 4 was revealed by fiber-FISH using the mitochondrial-related repetitive sequences, BAC-E38 and CsCent1. These showed the former sequences being integrated into the latter in multiple regions. The data presented here are useful resources for comparative genomics and cytogenetics of Cucumis and, in particular, the ongoing genome sequencing project of cucumber.
Similar content being viewed by others
Abbreviations
- BAC:
-
Bacterial artificial chromosome
- CCD:
-
Charge-coupled device
- CTAB:
-
Cetyltrimethylammonium bromide
- DAPI:
-
4′,6-Diamidino-2-phenylindole
- FISH:
-
Fluorescence in situ hybridization
- FITC:
-
Fluorescein isothiocyanate
- NOR:
-
Nucleolar-organizing region
- PI:
-
Propidium iodide
References
Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucl Acids Res 27:573–580
Blanchard JL, Lynch M (2000) Why do organellar genes end up in the nucleus? Trends Genet 16:315–320
Bradley RD, Wichman HA (1994) Rapidly evolving repetitive DNAs in a conservative genome: a test of factors that affect chromosomal evolution. Chromosome Res 2:354–360
Brennicke A, Hemleben V (1983) Sequence analysis of the cloned Cucumis melo highly repetitive satellite DNA. Z Naturforsch 38:1062–1065
Cerbah M, Coulaud J, Siljak-Yakovlev S (1998) rDNA organization and evolutionary relationships in the genus Hypochaeris (Asteraceae). J Hered 89:312–318
Cheng Z, Robin-Buell C, Wing RA, Gu M, Jiang JM (2001) Toward a cytological characterization of the rice genome. Genome Res 11:2133–2141
Cheng Z, Dong F, Langdon T, Ouyang S, Robin-Buell C, Gu M, Blattner FR, Jiang JM (2002) Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell 14:1691–1704
Choo KH (2001) Domain organization at the centromere and neocentromere. Dev Cell 1:165–177
Choo KH, Vissel B, Brown R, Filby RG, Earle E (1988) Homologous alpha satellite sequences on human acrocentric chromosomes with selectivity for chromosomes 13, 14, and 21: implications for recombination between non homologs and Robertsonian translocations. Nucl Acids Res 16:1273–1284
de Jong JH, Fransz P, Zabel P (1999) High resolution FISH in plants—techniques and applications. Trends Plant Sci 4:258–263
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 fibers. Plant J 9:421–430
Fransz PF, Armstrong S, Alonso-Blanco C, Fischer TC, Torres-Ruiz RA, Jones GH (1998) Cytogenetics for the model system Arabidopsis thaliana. Plant J 13:867–876
Fransz PF, Armstrong S, de Jong JH, Parnell LD, van Drunen C, Dean C, Zabel P, Bisseling T, Jones GH (2000) Integrated cytogenetic map of chromosome arm 4 S of A. thaliana: structural organization of heterochromatic knob and centromere region. Cell 100:367–376
Fry K, Salser W (1977) Nucleotide sequences of HS-alpha satellite DNA from kangaroo rat Dipodomys ordii and characterization of similar sequences in other rodents. Cell 12:1069–1084
Ganal M, Hemleben V (1988) Insertion and amplification of a DNA sequence in satellite DNA of Cucumis sativus L. (Cucumber). Theor Appl Genet 75:357–361
Ganal M, Riede I, Hemleben V (1986) Organization and sequence analysis of two related satellite DNAs in cucumber (Cucumis sativus L.). J Mol Evol 23:23–30
Garagna S, Zuccotti M, Redi CA, Capanna E (1997) Trapping speciation. Nature 390:241–242
Garagna S, Marziliano N, Zuccotti M, Searle JB, Capanna E, Redi CA (2001) Pericentromeric organization at the fusion point of mouse Robertsonian translocation chromosomes. Proc Natl Acad Sci U S A 98:171–175
Gerlach WL, Bedbrook JR (1979) Cloning and characterization of ribosomal RNA genes from wheat and barley. Nucleic Acids Res 7:1869–1885
Hall KJ, Parker JS (1995) Stable chromosome fission associated with rDNA mobility. Chromosome Res 3:417–422
Han YH, Zhang Z, Liu JH, Lu JY, Huang SW, Jin WW (2008) Distribution of the tandem repeat sequences and karyotyping in cucumber (Cucumis sativus L.) by fluorescence in situ hybridization. Cytogenet Genome Res 122:90–98
Han YH, Zhang Z, Liu C, Huang S, Jiang JM, Jin WW (2009) Centromere repositioning in cucurbit species: Implication of the genomic impact from centromere activation and inactivation. Proc Natl Acad Sci U S A 106:14937–14941
Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293:1098–102
Hirai H, Yamamoto MT, Ogura K, Satta Y, Yamada M, Taylor RW, Imai HT (1995) Multiplication of 28S rDNA and NOR activity in chromosome evolution among ants of the Myrmecia pilosula species complex. Chromosoma 103:171–178
Hirai H, Yamamoto MT, Taylor RW, Imai HT (1996) Genomic dispersion of 28S rDNA during karyotypic evolution in the ant genus Myrmecia (Formicidae). Chromosoma 105:190–196
Huang S, Li R, Zhang Z et al (2009) The genome of the cucumber, Cucumis sativus L. Nat Genet 41:1275–1281
Jackson SA, Wang MI, Goodman HM, Jiang JM (1998) Application of fiber-FISH in physical mapping of Arabidopsis thaliana. Genome 41:566–572
Jiang JM, Gill BS (1994) New 18S. 26S ribosomal RNA gene loci: chromosomal landmarks for the evolution of polyploid wheats. Chromosoma 103:179–185
Jiang JM, Gill BS (2006) Current status and the future of fluorescence in situ hybridization (FISH) in plant genome research. Genome 49:1057–1068
Jiang JM, Birchler J, Parrott W, Dawe R (2003) A molecular view of plant centromeres. Trends Plant Sci 8:570–575
Jo SH, Koo DH, Kim JF, Hur CG, Lee S, Yang TJ, Kwon SY, Choi D (2009) Evolution of ribosomal DNA-derived satellite repeat in tomato genome. BMC Plant Bio 9:42
Kato A, Lamb JC, Birchler JA (2004) Chromosome painting using repetitive DNA sequences as probes for somatic chromosome identification in maize. Proc Natl Acad Sci U S A 101:13554–13559
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
Koo DH, Choi HW, Cho J, Hur Y, Bang JW (2005) A high-resolution karyotype of cucumber (Cucumis sativus L. 'Winter Long') revealed by C-banding, pachytene analysis, and RAPD-aided fluorescence in situ hybridization. Genome 48:534–540
Li YC, Lee C, Sanoudou D, Hsu TH, Li SY, Lin CC (2000) Interstitial colocalization of two cervid satellite DNAs involved in the genesis of the Indian muntjac karyotype. Chromosome Res 8:363–373
Lilly JW, Havey MJ (2001) Small, repetitive DNAs contribute significantly to the expanded mitochondrial genome of cucumber. Genetics 159:317–328
Lin X, Kaul S, Rounsley S, Shea TP et al (1999) Sequence and analysis of chromosome 2 of the plant Arabidopsis thaliana. Nature 402:761–768
Maluszynska J, Heslop-Harrison JS (1991) Localization of tandemly repeated DNA sequences in Arabidopsis thaliana. Plant J 1:159–166
Nam YW, Lee JR, Song KH, Lee MK, Robbins MD, Chung SM, Staub JE, Zhang HB (2005) Construction of two BAC libraries from cucumber (Cucumis sativus L.) and identification of clones linked to yield component quantitative trait loci. Theor Appl Genet 111:150–161
Page SL, Shin JC, Han JY, Choo KHA, Shaffer LG (1996) Breakpoint diversity illustrates distinct mechanisms for Robertsonian translocation formation. Hum Mol Genet 5:1279–1288
Parsons JD (1995) Miropeats: graphical DNA sequence comparisons. Comput Appl Biosci 11:615–619
Peterson DG, Lapitan NLV, Stack SM (1999) Localization of single- and low-copy sequences on tomato synaptonemal complex spreads using fluorescence in situ hybridization (FISH). Genetics 152:427–439
Pinkel D, Straume T, Gray JW (1986) Cytogenetic analysis using quantitative, high-sensitivity, fluorescence hybridization. Proc Natl Acad Sci U S A 83:2934–2938
Plohl M, Luchetti A, Mestrović N, Mantovani B (2008) Satellite DNAs between selfishness and functionality: structure, genomics and evolution of tandem repeats in centromeric (hetero) chromatin. Gene 409:72–82
Rogers SO, Bendich AJ (1988) Extraction of milligram amounts of DNA from fresh, herbarium and mummified plant tissue. Plant Mol Biol Rep 5:69–76
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
Schaefer H, Heibl C, Renner SS (2009) Gourds afloat: A dated phylogeny reveals an Asian origin of the gourd family (Cucurbitaceae) and numerous oversea dispersal events. Proc R Soc B 276:843–851
Shan F, Yan G, Plummer A (2003) Cyto-evolution of Boronia genomes revealed by fluorescence in situ hybridization with rDNA probes. Genome 46:507–513
Stahl A, Luciani JM, Hartung M, Devictor M, Berge Lefranc JL, Guichaoua M (1983) Structural basis for Robertsonian translocations in man: association of ribosomal genes in the nucleolar fibrillar center in meiotic spermatocytes and oocytes. Proc Natl Acad Sci U S A 80:5946–5950
Stupar RM, Lilly JW, Town CD, Cheng Z, Kaul S, Buell CR, Jiang JM (2001) Complex mtDNA constitutes and approximate 620 kb insertion on Arabidopsis thaliana chromosome 2: implication of potential sequencing errors caused by large-unit repeats. Proc Natl Acad Sci U S A 98:5099–5103
Sullivan BA, Jenkins LS, Karson EM, Leana-Cox J, Schwartz S (1996) Evidence for structural heterogeneity from molecular cytogenetic analysis of dicentric Robertsonian translocations. Am J Hum Genet 59:167–175
Talbert PB, Masuelli R, Tyagi AP, Comai L, Henikoff S (2002) Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell 14:1053–1066
Ugarkovic D, Plohl M (2002) Variation in satellite DNA profiles—causes and effects. EMBO J 21:5955–5959
Ward BL, Anderson RS, Bendich AJ (1981) The mitochondrial genome is large and variable in a family of plants (Cucurbitaceae). Cell 25:793–803
Wevrick R, Willard HF (1989) Long-range organization of tandem arrays of a satellite DNA at the centromeres of human chromosomes: high frequency array-length polymorphism and meiotic stability. Proc Natl Acad Sci U S A 86:9394–9398
Wichman HA, Payne CT, Ryder OA, Hamilton MJ, Maltbie M, Baker RJ (1991) Genomic distribution of heterochromatic sequences in equids: implications to rapid chromosomal evolution. J Hered 82:369–377
Acknowledgements
We are grateful to Dr. Jiming Jiang for his valuable comments on this manuscript. This work was supported by a grant from the Korea Research Foundation (KRF-2000-DP0401) to YH.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Responsible Editor: Herbert Macgregor.
Electronic supplementary materials
Below is the link to the electronic supplementary material.
ESM Table 1
Repeats on BAC-E38 BAC sequence analyzed by RepeatMasker v1.162 (2005/04/14) run with cross match version 0.990329, RepBase Update 9.11(database version 20050112) (DOC 57 kb)
ESM Table 2
Repeats on BAC-E38 analyzed by Tandem Repeats Finder Version 3.21 (parameters 2 7 7 80 10 50 500) (DOC 56 kb)
ESM Table 3
Repeats on BAC-E38 BAC sequence analyzed by Miropeats (threshold value = 100) (DOC 37 kb)
ESM Table 4
Characterization of nine ORFs predicted by FGENESH in BAC-E38 (DOC 34 kb)
ESM Fig. 1
(DOC 308 kb)
Rights and permissions
About this article
Cite this article
Koo, DH., Nam, YW., Choi, D. et al. Molecular cytogenetic mapping of Cucumis sativus and C. melo using highly repetitive DNA sequences. Chromosome Res 18, 325–336 (2010). https://doi.org/10.1007/s10577-010-9116-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10577-010-9116-0