Abstract
The B24 chromosome in the Torrox population of the grasshopper Eyprepocnemis plorans is recurrently attached to a nucleolus in diplotene cells, indicating the activity of its distally located ribosomal DNA (rDNA). The frequency of males expressing the B chromosome nucleolus organizer region (B-NOR) almost doubled in 4 years. The likelihood of expressing the B-NOR increased with the B number and, in males expressing it, about 20% of their cells showed a nucleolus attached to the B. When active, the B-NOR contributed more than 25% of total cell nucleolar area (NA). Within males expressing the B-NOR, total cell NA did not differ between cells showing the active or inactive B-NOR, suggesting that total cell NA is tightly regulated in this species. However, this parameter tended to increase in this population from 1999 to 2004, in parallel to the neutralization process which is taking place in this population. Finally, an analysis of A chromosome NOR interdependence for activity revealed a positive correlation among autosomes but a negative correlation between autosomes and the X chromosome, the manifestation of which depends on B-NOR activity. These results are discussed in the context of the nucleolus as a sensor of the stress caused by parasitic B chromosomes.
Similar content being viewed by others
References
Bakkali M, Cabrero J, López-León MD, Perfectti F, Camacho JPM (2001) Population differences in the expression of nucleolus organizer regions in the grasshopper Eyprepocnemis plorans. Protoplasma 217:185–190
Cabrero J, Camacho JPM (2008) Location and expression of ribosomal RNA genes in grasshoppers: abundance of silent and cryptic loci. Chromosome Res 16:595–607
Cabrero J, Alché JD, Camacho JPM (1987) Effects of B chromosomes on the activity of Nucleolar Organizer Regions in the grasshopper Eyprepocnemis plorans. Activation of a latent Nucleolar Organizer Region on a B chromosome fused to an autosome. Genome 29:116–121
Cabrero J, Perfectti F, Gómez R, Camacho JPM, López-León MD (2003) Population variation in the A chromosome distribution of satellite DNA and ribosomal DNA in the grasshopper Eyprepocnemis plorans. Chromosome Res 11:375–381
Cabrero J, Teruel M, Carmona FD, Jiménez R, Camacho JPM (2007) Histone H3 lysine 9 acetylation pattern suggests that X and B chromosomes are silenced during entire male meiosis in a grasshopper. Cytogenet Genome Res 119:135–142
Camacho JPM (2004) B chromosomes in the eukaryote genome. Karger, Basel
Camacho JPM (2005) B chromosomes. In: Gregory TR (ed) The evolution of the genome. Elsevier, San Diego, pp 223–286
Camacho JPM, Shaw MW, López-León MD, Pardo MC, Cabrero J (1997) Population dynamics of a selfish B chromosome neutralized by the standard genome in the grasshopper Eyprepocnemis plorans. Amer Nat 149:1030–1050
Camacho JPM, Bakkali M, Corral JM, Cabrero J, López-León MD, Aranda I, Martín-Alganza A, Perfectti F (2002) Host recombination is dependent on the degree of parasitism. Proc Roy Soc Lond B 269:2173–2177
Caperta AD, Neves N, Viegas W, Pikaard CS, Preuss S (2007) Relationships between transcription, silver staining, and chromatin organization of nucleolar organizers in Secale cereale. Protoplasma 232:55–59
Caspersson T (1950) Cell growth and cell function, a cytochemical study. WW Norton, New York
Earley K, Lawrence RJ, Pontes O, Reuther R, Enciso AJ, Silva M, Neves N, Gross M, Viegas W, Pikaard CS (2006) Erasure of histone acetylation by Arabidopsis HDA6 mediates large-scale gene silencing in nucleolar dominance. Genes Dev 20:1283–1293
Grummt I (2003) Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. Genes Dev 17:1691–1702
Grummt I (2007) Different epigenetic layers engage in complex crosstalk to define the epigenetic state of mammalian rRNA genes. Hum Mol Genet 16 Spec No 1:R21–R27
Hiscox JA (2007) RNA viruses: hijacking the dynamic nucleolus. Nat Rev Microbiol 5:119–127
Huang S, Rothblum LI, Chen D (2006) Ribosomal chromatin organization. Biochem Cell Biol 84:444–449
Hudson LA, Ciborowski JJH (1996) Teratogenic and genotoxic responses of larval Chironomus salinarius group (Diptera: Chironimidae) to contaminated sediment. Environ Toxicol Chem 15:1375–1381
Jones RN, Viegas W, Houben A (2008) A century of B chromosomes in plants: So what? Annals of Botany 101:767–775
Karpen GH, Schaefer JE, Laird CD (1988) A Drosophila rRNA gene located in euchromatin is active in transcription and nucleolus formation. Genes Dev 2:1745–1763
Laferte A, Favry E, Sentenac A, Riva M, Carles C, Chedin S (2006) The transcriptional activity of RNA polymerase I is a key determinant for the level of all ribosome components. Genes Dev 20:2030–2040
Langerstedt S (1949) Cytological studies on the protein metabolism of the liver in the rat. Acta Anat Suppl 9:1–140
Lawrence RJ, Pikaard CS (2004) Chromatin turn ons and turn offs of ribosomal RNA genes. Cell Cycle 3:880–883
Lawrence RJ, Earley K, Pontes O, Silva M, Chen ZJ, Neves N, Viegas W, Pikaard CS (2004) A concerted DNA methylation/histone methylation switch regulates rRNA gene dosage control and nucleolar dominance. Mol Cell 13:599–609
Leach C, Houben A, Field B, Pistrick K, Demidov D, Timmis J (2005) Molecular evidence for transcription of genes on a B chromosome in Crepis capillaris. Genetics 171:269–278
Lewis MS, Pikaard CS (2001) Restricted chromosomal silencing in nucleolar dominance. Proc Natl Acad Sci USA 98:14536–14540
Lewis MS, Cheverud JM, Pikaard CS (2004) Evidence for nucleolus organizer regions as the units of regulation in nucleolar dominance in Arabidopsis thaliana interecotype hybrids. Genetics 167:931–939
Li J, Santoro R, Koberna K, Grummt I (2005) The chromatin remodelling complex NoRC controls replication timing of rRNA genes. EMBO J 24:120–127
López-León MD, Cabrero J, Camacho JPM (1991) A nucleolus Organizer Region in a B chromosome inactivated by DNA methylation. Chromosoma 100:134–138
López-León MD, Cabrero J, Camacho JPM (1995a) Changes in DNA methylation during development in the B chromosome NOR of the grasshopper Eyprepocnemis plorans. Heredity 74:296–302
López-León MD, Cabrero J, Camacho JPM (1995b) Changes in NOR activity pattern in the presence of supernumerary heterochromatin in the grasshopper Eyprepocnemis plorans. Genome 38:68–74
López-León MD, 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
López-León MD, Cabrero J, Dzyubenko VV, Bugrov AG, Karamysheva TV, Rubtsov NB, Camacho JPM (2008) Differences in ribosomal DNA distribution on A and B chromosomes between eastern and western populations of the grasshopper Eyprepocnemis plorans plorans. Cytogenet Genome Res 121:260–265
Matyasek R, Tate JA, Lim YK, Srubarova H, Koh J, Leitch AR, Soltis DE, Soltis PS, Kovarik A (2007) Concerted evolution of rDNA in recently formed Tragopogon allotetraploids is typically associated with an inverse correlation between gene copy number and expression. Genetics 176:2509–2519
Morais-Cecilio L, Delgado M, Jones R, Viegas W (2000) Modification of wheat rDNA loci by rye B chromosomes: a chromatin organization model. Chromosome Res 8:341–351
Mosgoeller W (2004) Nucleolar ultrastructure in vertebrates. In: Olson MOJ (ed) The Nucleolus. Kluwer, New York, pp 10–20
Moss T, Stefanovsky VY (2002) At the center of eukaryotic life. Cell 109:545–548
Muñoz E, Perfectti F, Martín-Alganza A, Camacho JPM (1998) Parallel effects of a B chromosome and a mite that decrease female fitness in the grasshopper Eyprepocnemis plorans. Proc Roy Soc Lond B 265:1903–1909
Nakamoto K, Ito A, Watabe K, Koma Y, Asada H, Yoshikawa K, Shinomura Y, Matsuzawa Y, Nojima H, Kitamura Y (2001) Increased expression of a nucleolar Nop5/Sik family member in metastatic melanoma cells: evidence for its role in nucleolar sizing and function. Am J Pathol 159:1363–1374
Nogi Y, Yano R, Nomura M (1991) Synthesis of large rRNAs by RNA polymerase II in mutants of Saccharomyces cerevisiae defective in RNA polymerase I. Proc Natl Acad Sci USA 88:3962–3966
Olson MOJ (2004) Sensing cellular stress: another new function for the nucleolus? Sci STKE 2004:e10
Pebusque MJ, Seite R (1981) Electron microscopic studies of silver-strained proteins in nucleolar organizer regions: location in nucleoli of rat sympathetic neurons during light and dark periods. J Cell Sci 51:85–94
Perfectti F, Corral JM, Mesa JA, Cabrero J, Bakkali M, López-León MD, Camacho JPM (2004) Rapid suppression of drive for a parasitic B chromosome. Cytogenet Genome Res 106:338–343
Pikaard CS (2000) The epigenetics of nucleolar dominance. Trends Genet 16:495–500
Preuss S, Pikaard CS (2007) rRNA gene silencing and nucleolar dominance: insights into a chromosome-scale epigenetic on/off switch. Biochim Biophys Acta 1769:383–392
Rasband WS (1997) ImageJ, volume http://rsb.info.nih,gov/ij. Bethesda, Maryland, USA: U. S. National Institutes of Health
Roussel P, Andre C, Comai L, Hernandez-Verdun D (1996) The rDNA transcription machinery is assembled during mitosis in active NORs and absent in inactive NORs. J Cell Biol 133:235–246
Roussel P, Belenguer P, Amalric F, Hernandez-Verdun D (1992) Nucleolin is an Ag-NOR protein; this property is determined by its amino-terminal domain independently of its phosphorylation state. Exp Cell Res 203:259–269
Roussel P, Hernandez-Verdun D (1994) Identification of Ag-NOR proteins, markers of proliferation related to ribosomal gene activity. Exp Cell Res 214:465–472
Rudra D, Warner JR (2004) What better measure than ribosome synthesis? Genes Dev 18:2431–2436
Rufas JS, Iturra P, de Souza W, Esponda P (1982) Simple silver staining procedure for the localization of nucleolus and nucleolar organizer under light and electron microscopy. Arch Biol 93:267–274
Santoro R (2005) The silence of the ribosomal RNA genes. Cell Mol Life Sci 62:2067–2079
Santoro R, Li J, Grummt I (2002) The nucleolar remodelling complex NoRC mediates heterochromatin formation and silencing of ribosomal gene transcription. Nat Genet 32:393–396
Sollner-Webb B, Tower J (1986) Transcription of cloned eukaryotic ribosomal RNA genes. Annu Rev Genet 55:801–830
Teruel M, Cabrero J, Perfectti F, Camacho JPM (2007) Nucleolus size variation during meiosis and NOR activity of a B chromosome in the grasshopper Eyprepocnemis plorans. Chromosome Res 15:755–765
Tsai RY, McKay RD (2005) A multistep, GTP-driven mechanism controlling the dynamic cycling of nucleostemin. J Cell Biol 168:179–184
Tsang CK, Bertram PG, Ai W, Drenan R, Zheng XF (2003) Chromatin-mediated regulation of nucleolar structure and RNA Pol I localization by TOR. EMBO J 22:6045–6056
Tuma RS (2005) A GTP signal to the nucleolus. J Cell Biol 168:172
Warner JR (1999) The economics of ribosome biosynthesis in yeast. Trends Biochem Sci 24:437–440
Weisenberger D, Scheer U (1995) A possible mechanism for the inhibition of ribosomal RNA gene transcription during mitosis. J Cell Biol 129:561–575
Zhou Y, Santoro R, Grummt I (2002) The chromatin remodelling complex NoRC targets HDAC1 to the ribosomal gene promoter and represses RNA polymerase I transcription. EMBO J 21:4632–4640
Zurita S, Cabrero J, López-León MD, Camacho JPM (1998) Polymorphism regeneration for a neutralized selfish B chromosome. Evolution 52:274–277
Acknowledgements
This study was supported by FEDER funds and grants from the Spanish Ministerio de Ciencia e Innovación (CGL2006-06307) and Plan Andaluz de Investigación (CVI-1664). MT was supported by a fellowship (FPI) from the Spanish Ministerio de Ciencia e Innovación. We also thank David Nesbitt for English corrections.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by I. Grummt.
Rights and permissions
About this article
Cite this article
Teruel, M., Cabrero, J., Perfectti, F. et al. Quantitative analysis of NOR expression in a B chromosome of the grasshopper Eyprepocnemis plorans. Chromosoma 118, 291–301 (2009). https://doi.org/10.1007/s00412-008-0197-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00412-008-0197-x