Summary
Fluorescence in situ hybridization revealed the presence of ribosomal RNA genes in paracentromeric regions of all A chromosomes and in the distal half of B chromosomes in embryonic cells from Moroccan specimens of the grasshopperEyprepocnemis plorans. The expression of these genes was monitored by the presence of nucleoli attached to each chromosome bivalent in diplotene cells from males collected from two different Moroccan populations and was compared to previous data of Spanish populations. Whereas only the nucleolus organizer regions (NORs) on S9–S11 and X chromosomes were active in the Spanish specimens. Moroccan individuals showed NOR activity in all chromosomes. The rRNA genes on the B chromosome were inactive in both populations. The S9 and S10 NORs were less active in Moroccan specimens than in Spanish specimen, which might be partly explained by the negative interdependence for expression of the S10 NOR with respect to those on L2 and X chromosomes. On the other hand, the X NOR was more active in Moroccan specimens than in Spanish specimens, and this might be partly due to the positive effect that the presence of B chromosomes has on the expression of this NOR. The implications of these observations on current models of NOR activity regulation are discussed.
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Abbreviations
- NOR:
-
nucleolus organizer region
References
Bakkali M, Cabrero J, López-León MD, Perfectti F, Camacho JPM (1999) The B chromosome polymorphism of the grasshopperEyprepocnemis plorans in north Africa I: B variants and frequency. Heredity 83: 428–434
Cabrero J, Alché JD, Camacho JPM (1987) Effects of B chromosome on the activity of nucleolus organizer regions in the grasshopperEyprepocnemis plorans: activation of a latent nucleolus organizer region on a B chromosome fused to an autosome. Genome 29: 116–121
—, López-León MD, Bakkali M, Camacho JPM (1999) Common origin of B chromosome variants in the grasshopperEyprepocnemis plorans. Heredity 83: 435–439
Camacho JPM, Cabrero J, Viseras E, López-León MD, Navas-Castillo J, Alché JD (1991) G banding in two species of grasshopper and its relationship to C, N, and fluorescence banding techniques. Genome 34: 638–643
—, Sharbel TF, Beukeboom LW (2000) B chromosome evolution. Philos Trans R Soc Lond Ser B 355: 163–178
Caspersson T (1950) Cell growth and cell function: a cytochemical study. WW Norton and Co, New York
De Capoa A, Felli MP, Baldini A, Rocchi M, Archidiacono N, Aleixander C, Miller OJ (1988) Relationship between the number and function of ribosomal genes. Human Genet 79: 301–304
Evans HJ, Buckland RA, Pardue ML (1974) Location of the genes coding for 18S and 28S ribosomal RNA in the human genome. Chromosoma 48: 405–426
Galleti PM Jr, Barbosa da Silva E, Germinaro RJ (1985) A multiple NOR system in the fishSerrasalmus spilopleura (Serrasalminae, Characidae). Rev Brasil Genet 8: 479–484
Henderson AS, Eicher EM, Yu MT, Atwood KC (1976) Variation in ribosomal RNA gene number in mouse chromosomes. Cytogenet Cell Genet 17: 307–316
John B, Lewis KR (1965) Genetic speciation in the grasshopperEyprepocnemis plorans. Chromosoma 16: 548–578
King M, Contreras N, Honeycutt RL (1990) Variation within and between nucleolus organizer regions in Australian hylid frogs (Anura) shown by 18S + 28S in situ hybridization. Genetica 80: 17–29
Leitch IJ, Heslop-Harrison JS (1992) Physical mapping of the 18S — 5.8S — 26S rRNA genes in barley by in situ hybridisation. Genome 35: 1013–1018
López-León MD, Cabrero J, Camacho JPM (1991) A nucleolus organizer region in a B chromosome inactivated by DNA methylation. Chromosoma 100: 134–138
—, Neves N, Schwarzacher T, Heslop-Harrison JS, Hewitt GM, Camacho JPM (1994) Possible origin of a B chromosome deduced from its DNA composition using double FISH technique. Chromosome Res 2: 87–92
—, Cabrero J, Camacho JPM (1995) Changes in NOR activity pattern in the presence of supernumerary heterochromatin in the grasshopperEyprepocnemis plorans. Genome 38: 68–74
Mellink CHM, Bosma AA, De Haan NA (1994) Variation in size of Ag-NORs and fluorescent rDNA in situ hybridization signals in six breeds of domestic pig. Hereditas 120: 141–149
Miller L, Brown DD (1969) Variation in the activity of nucleolus organizes and their ribosomal gene content. Chromosoma 28: 430–444
Rice WR (1989) Analysing tables of statistical tests. Evolution 43: 223–225
Rufas JS, Iturra P, De Souza W, Esponda P (1982) Simple silver staining procedure for the localization of nucleolus and nucleolus organizes under light and electron microscopy. Arch Biol 93: 267–276
Salcedo FJ, Viseras E, Camacho JPM (1988) The B chromosomes ofLocusta migratoria III: effects on the activity of nucleolar organizer regions. Genome 30: 387–394
Sánchez A, Burgos M, Jiménez R, Díaz de la Guardia R (1989) Quantitative analysis of silver staining of the nucleolus organizing region inEliomys quercinus. Genome 32: 978–982
Sasaki M, Nishida C, Kodama Y (1986) Characterization of silver stained nucleolus organizer regions (AG-NORs) in 16 inbred strains of the Norway rat,Rattus norvegicus. Cytogenet Cell Genet 41: 83–88
Schmidtke J, Schulte B, Kuhl P, Engel W (1976) Gene action in fish of tetraploid origin V: Cellular RNA and protein content and enzyme activities in cyprinid, clupeoid, and salmonoid species. Biochem Genet 14: 975–980
Shubert I, Künzel G (1990) Position dependent NOR activity in barley. Chromosoma 99: 352–359
Sinclair JH, Carrol CR, Humphrey RR (1974) Variation in rDNA redundance level and NOR length in normal and variant lines of the Mexican axolotl. J Cell Sci 15: 239–257
Stitou S, Díaz de la Guardia R, Jiménez R, Burgos M (2000) Inactive ribosomal cistrons are spread throughout the B chromosomes ofRattus rattus (Rodentia, Muridae): implications for their origin and evolution. Chromosome Res 8: 305–311
Suzuki H, Kurihara Y, Kanehisa T, Moriwaki K (1990) Variation in the distribution of the silver staining nucleolus organizer regions on the chromosomes of the wild mouse,Mus musculus. Mol Biol Evol 7: 271–282
Wachtler F, Hopman AH, Wiegant J, Schwarzacher HG (1986) On the position of nucleolus organizer regions (NORs) in interphase nuclei: studies with a new, non autoradiographic in situ hybridization method. Exp Cell Res 167: 227–240
Yoder JA, Walsh CP, Bestor TH (1997) Cytosine methylation and the ecology of intragenomic parasites. Trends Genet 13: 335–340
Zatsepina OV, Schofer C, Weipoltshammer K, Mosgoeller W, Almeder M, Stefanova VN, Jordan EG, Wachtler F (1996) The RNA-polymerase-I transcription factor UF and rDNA are located at the same major sites in both interphase and mitotic pig embryonic kidney. Cytogenet Cell Genet 73: 274–278
Zurita F, Jiménez R, Burgos M, Díaz de la Guardia R (1998) Sequential silver staining and in situ hybridization reveal a direct association between rDNA levels and the expression of homologous nucleolus organizing regions: a hypothesis for NOR structure and function. J Cell Sci 111: 1433–1439
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Bakkali, M., Cabrero, J., López-León, M.D. et al. Population differences in the expression of nucleolus organizer regions in the grasshopperEyprepocnemis plorans . Protoplasma 217, 185–190 (2001). https://doi.org/10.1007/BF01283399
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DOI: https://doi.org/10.1007/BF01283399