Cytosine methylation and nucleolar dominance in cereal hybrids

Houchins, Katherine; O’Dell, M.; Flavell, R. B.; Gustafson, J. P.

doi:10.1007/s004380050500

Cited by 65 publications

(38 citation statements)

References 34 publications

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“…and C.S.P., unpublished work). These results argue against models in which hypermethylation of underdominant rRNA gene promoters directly blocks transcription factor binding (44). However, it is possible that methylation acts indirectly via recruitment of methylcytosine-binding protein complexes that include histone deacetylase activity (45,46).…”

Section: Discussioncontrasting

confidence: 41%

Gene dosage and stochastic effects determine the severity and direction of uniparental ribosomal RNA gene silencing (nucleolar dominance) in Arabidopsis allopolyploids

Chen

Comai

Pikaard

1998

Proc. Natl. Acad. Sci. U.S.A.

209

169

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Nucleolar dominance is an epigenetic phenomenon in which one parental set of ribosomal RNA (rRNA) genes is silenced in an interspecific hybrid. In natural Arabidopsis suecica, an allotetraploid (amphidiploid) hybrid of Arabidopsis thaliana and Cardaminopsis arenosa, the A. thaliana rRNA genes are repressed. Interestingly, A. thaliana rRNA gene silencing is variable in synthetic Arabidopsis suecica F 1 hybrids. Two generations are needed for A. thaliana rRNA genes to be silenced in all lines, revealing a species-biased direction but stochastic onset to nucleolar dominance. Backcrossing synthetic A. suecica to tetraploid A. thaliana yielded progeny with active A. thaliana rRNA genes and, in some cases, silenced C. arenosa rRNA genes, showing that the direction of dominance can be switched. The hypothesis that naturally dominant rRNA genes have a superior binding affinity for a limiting transcription factor is inconsistent with dominance switching. Inactivation of a species-specific transcription factor is argued against by showing that A. thaliana and C. arenosa rRNA genes can be expressed transiently in the other species. Transfected A. thaliana genes are also active in A. suecica protoplasts in which chromosomal A. thaliana genes are repressed. Collectively, these data suggest that nucleolar dominance is a chromosomal phenomenon that results in coordinate or cooperative silencing of rRNA genes.Nucleolar dominance was among the first recognized epigenetic phenomena, discovered in interspecific hybrids in the plant genus Crepis. Navashin noted secondary constrictions at metaphase on D chromosomes inherited from one Crepis species, but not on the D chromosome from the other species (1, 2). Navashin's contemporary, McClintock, showed that these secondary constrictions are sites where nucleoli were organized in the preceding interphase (3). Decades later, nucleolus organizer regions (NORs) were identified as loci where genes encoding the precursor of the 18S, 5.8S, and 25-28S ribosomal RNAs are tandemly arrayed (4-7). Thus, nucleolar dominance was shown ultimately to result from uniparental rRNA gene expression (8).Nucleolar dominance occurs throughout the plant and animal kingdoms (9, 10) via mechanisms that remain unclear. Navashin noted that dominant NOR-bearing chromosomes could be contributed through the pollen or egg (2), ruling out maternal or paternal effects. A dominant D chromosome could also be contributed as part of an incomplete chromosome set. In Drosophila melanogaster ϫ Drosophila simulans hybrids, the D. melanogaster NORs on the X and Y chromosomes are dominant over the single NOR on the D. simulans X (11). In hybrid XO males lacking a D. melanogaster sex chromosome, but containing all autosomes, the D. simulans NOR is active. These results indicate that NOR-bearing chromosomes must be present for nucleolar dominance to occur.

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Section: Discussioncontrasting

confidence: 41%

Gene dosage and stochastic effects determine the severity and direction of uniparental ribosomal RNA gene silencing (nucleolar dominance) in Arabidopsis allopolyploids

Chen

Comai

Pikaard

1998

Proc. Natl. Acad. Sci. U.S.A.

209

169

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“…Therefore, the initial effects may depend on the particular enhancer region and possibly also on the cell type. In the case described here, methylation of a short promoter region suffices to alter the tissue specificity; in other cases, methylation of even single cytosines can be effective (56,75). It seems possible that such regional methylation could allow for a stable control of promoter specificity in contrast to the general on͞off control usually associated with gene silencing.…”

Section: Discussionmentioning

confidence: 95%

Tissue-specific silencing of a transgene in rice

Klöti

Potrykus

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

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In a transgenic rice line, a ␤-glucuronidase reporter gene under the control of the rice tungro bacilliform virus promoter became gradually methylated, and gene activity was lost concomitantly. Methylation was observed only in the homozygous offspring and was initially restricted to the promoter region and accompanied by loss of expression in the vascular bundle tissue only. This expression pattern was similar to that of a promoter with a deletion of a vascular bundle expression element. The gene activity could be reestablished by treatment with 5-azacytidine. Methylation per se did not inhibit the binding to the promoter region of protein factors which also bound to the unmethylated sequence. Instead, promoter methylation enabled the alternative binding of a protein with specificity for sequence and methylation. In further generations of homozygous offspring the methylation spread into the transcribed region and gene activity was completely repressed also in nonvascular cells. The results indicate that different stages are involved in DNA methylation-correlated gene inactivation, and that at least one of them may involve the attraction of a sequence and methylation-specific DNA-binding protein.

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“…Another well-studied example of inter-genomic suppression is the silencing of rye ribosomal RNA genes in the presence of the wheat genome. Cytosine methylation is involved in this silencing as suggested by reactivation of the rye ribosomal RNA genes upon treatment with 5-aza-cytidine and by the use of methylation-sensitive/-insensitive isoschizomers (Houchins et al, 1997). In addition to intergenomic suppression, dosage compensation for storage proteins was also observed in aneuploid series of wheat with doses of 0 to 6 for the storage proteincoding chromosome (Galili et al, 1986).…”

Section: Changes In Gene Expression (Genetic Diploidization)mentioning

confidence: 92%