Scrambled actin I gene in the micronucleus of <i>Oxytricha nova</i>

Prescott, David M.; Greslin, Arthur F.

doi:10.1002/dvg.1020130111

Cited by 65 publications

(53 citation statements)

References 7 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…These are the C2 gene (21), the R1 gene (30), and genes encoding actin I (12,13,29), ␤-TP (15, 26), ␣-TP (the ␣-subunit of the telomerebinding protein) (11,25), DNA polymerase ␣ (17, 24), and heat shock protein 70 (1,23). For each of the genes that has been sequenced in the present work, multiple micronuclear …”

Section: Resultsmentioning

confidence: 99%

See 1 more Smart Citation

Volatility of Internal Eliminated Segments in Germ Line Genes of Hypotrichous Ciliates

DuBois

Prescott

1997

Molecular and Cellular Biology

View full text Add to dashboard Cite

Germ line micronuclear genes in ciliated protozoa contain two types of interrupting sequences. Some genes contain introns, but internal eliminated segments (IESs) are much more prevalent. IESs are AT-rich DNA segments that separate macronucleus-destined segments (MDSs) in micronuclear genes. All IESs are excised and destroyed when a micronucleus develops into a macronucleus after each cell mating. IESs have no discernible function. Therefore, an investigation of the behavior of IESs in evolution has been undertaken to assess their possible significance. The IESs in the micronuclear gene encoding the ␤-subunit of the telomerebinding protein (␤-TP) are not conserved in number, position, sequence, or length during the evolution of four oxytrichid ciliates. In contrast, the scrambled pattern of MDSs and IESs of the micronuclear actin I gene has been conserved during evolution; however, the precise positions, sequences, and lengths of the IESs differ among species, and in some organisms the actin I gene contains an additional IES and MDS. Corresponding IESs in the actin I genes among the different organisms have shifted positions by 1 to 14 bp, presumably by a mutation-shifting mechanism, creating differences in the repeat sequences flanking IESs. Thus, conservation of a particular repeat sequence among species is not required for IES excision. The changes in IES number and position in the ␤-TP genes among ciliates are in sharp contrast to the stability of the intron position. Therefore, IESs are volatile, hypermutable elements that are inserted, removed, shifted, and modified continuously in the germ line through evolutionary time.Ciliated protozoa contain two classes of interruptions in their germ line (micronuclear) genes. Introns are present in some genes, although in general, ciliate genes are intron poor (reviewed in reference 27). Much more common are interruptions known as internal eliminated segments (or sequences) (IESs), first described for the hypotrichous ciliate Oxytricha nova (21). Occurrence of IESs is particularly high in germ line genes of ciliates of the order Hypotrichida. Collectively, a micronuclear genome in the oxytrichid hypotrichs (genera Oxytricha and Stylonychia) may contain a total of ϳ200,000 IESs, which are all AT rich (60 to 100% AT). Oxytrichid IESs range in size from 7 bp to several hundred base pairs and appear to be randomly distributed throughout micronuclear genes.A remarkable feature of IESs is their precise excision from genes, by an unknown mechanism, when a micronucleus develops into a macronucleus (somatic nucleus) after cell mating. DNA segments separated by IESs are called macronucleusdestined segments (or sequences) (MDSs). After IES excision, MDSs are spliced together to form transcriptionally active macronuclear genes. In some genes, IESs separate MDSs that are not in the orthodox order, and the MDSs must be unscrambled during development to form a functional gene. IES excision is presumed to require the repeat sequences (2 to 19 bp) that flank each IES. The repeats fla...

show abstract

Section: Resultsmentioning

confidence: 99%

“…Cell culture and nuclear isolations were described previously (29). Micronuclear and macronuclear pellets were suspended in Tris-EDTA, mixed with sodium dodecyl sulfate to 0.1%, and extracted three times with phenol and once with chloroform, and the resulting DNAs were precipitated in ethanol.…”

Section: Methodsmentioning

confidence: 99%

Volatility of Internal Eliminated Segments in Germ Line Genes of Hypotrichous Ciliates

DuBois

Prescott

1997

Molecular and Cellular Biology

View full text Add to dashboard Cite

show abstract

“…Stylonychia pustulata was isolated from the Roaring Fork River, Aspen, Colorado. All three were grown on Chlorogonium as described (4). Engelmanniella mobilis was a gift from W. Foissner (Universität Salzburg, Salzburg, Austria).…”

Section: Methodsmentioning

confidence: 99%

“…DNA Preparation. Macronuclei and micronuclei were isolated from 10-20 ml of packed cells as described (4). DNA was purified by phenol͞chloroform extractions.…”

Section: Methodsmentioning

confidence: 99%

Evolution of IESs and scrambling in the actin I gene in hypotrichous ciliates

Hogan

Hewitt

Orr

et al. 2001

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

Self Cite

View full text Add to dashboard Cite

Germ-line (micronuclear) genes in hypotrichous ciliates are interrupted by numerous, short, noncoding, AT-rich segments called internal eliminated segments, or IESs. IESs divide a gene into macronuclear destined segments, or MDSs. IESs are excised from micronuclear genes, and the MDSs are spliced when a micronuclear genome is processed into a macronuclear genome after cell mating. In the micronuclear version of the actin I gene intramolecular recombination between IESs during evolution has put MDSs into a scrambled disorder in some but not all hypotrichs. Studies using rDNA sequences to define phylogenetic relationships among eight hypotrichs suggests that evolution of the micronuclear actin I gene proceeds by successive addition of IESs in earlier diverging species, without MDS scrambling. Continued addition of IESs and recombination among IESs in later diverging species produced actin I genes with scrambled MDSs. Subsequent to MDS scrambling, additional IESs were inserted into the more recently evolved species. Thus, IES insertions and gene scrambling occur in a progressive manner during species evolution to produce micronuclear actin I genes of increasing structural complexity.G enes in micronuclear (germ-line) DNA of hypotrichous ciliates are interrupted by multiple, short, AT-rich, noncoding segments called internal eliminated segments, or IESs. IESs divide a gene into macronuclear destined segments, or MDSs. In some genes intramolecular recombination between IESs during evolution has disordered MDSs-i.e., MDSs have become scrambled. During development of a micronucleus into a new macronucleus after cell mating, IESs are spliced out of genes and MDSs are rearranged and ligated in the orthodox order to produce a transcribable gene (1). After MDS ligation the genes are excised from chromosomal DNA as individual, short DNA molecules, and all of the remaining DNA (spacer DNA), which accounts for Ϸ95% of the nucleotide sequence complexity in the micronuclear genome, is destroyed. Generally, one gene is present per molecule, but a small percentage of molecules may contain two genes (2) or even three genes (D.M.P., J. D. Prescott, and R. M. Prescott, unpublished observation).The significance of IESs in micronuclear genes is not understood, although it has been suggested that they facilitate evolution of new genes; recombination among IESs, which results in shuffling of MDSs, could conceivably create new, intergenic MDS combinations. Thus, the presence of scrambled MDSs in contemporary hypotrichs is a manifestation of intragenic MDS shuffling caught in evolutionary time. In addition, IES position within a gene can change (shift), which alters the sequence composition and size of MDSs in that gene (3), increasing further the versatility of MDS shuffling. At the very least, IES shifting and MDS scrambling by IES recombination, as reaffirmed in the data reported here, attest to an extraordinarily dynamic nature of the germ-line genome in hypotrichs over evolutionary time.This paper discusses the origin and evolution o...

show abstract

“…The order of recombination events does not matter in the simple hypothetical case shown here. Observed configurations of scrambled genes are considerably more complex and seem to be patterned in ways that reflect the avoidance of configurations in which nonproductive ordering of recombination events is possible; observed configurations also could reflect aspects of chromosome structure (Prescott and Greslin 1992), presumably by influencing the likelihood of events of developmental or mutational rearrangement. Nonetheless, the bias noted in the text will be strong even if the set of neutral, readily realizable configurations is only a tiny fraction of the conceivable configurations.…”

Section: The Evolution Of Scrambled Ciliate Genesmentioning

confidence: 99%

On the Possibility of Constructive Neutral Evolution

1999

View full text Add to dashboard Cite

Abstract. The neutral theory often is presented as a theory of "noise" or silent changes at an isolated "molecular level," relevant to marking the steady pace of divergence, but not to the origin of biological structure, function, or complexity. Nevertheless, precisely these issues can be addressed in neutral models, such as those elaborated here with regard to scrambled ciliate genes, gRNA-mediated RNA editing, the transition from selfsplicing to spliceosomal splicing, and the retention of duplicate genes. All of these are instances of a more general scheme of "constructive neutral evolution" that invokes biased variation, epistatic interactions, and excess capacities to account for a complex series of steps giving rise to novel structures or operations. The directional and constructive outcomes of these models are due not to neutral allele fixations per se, but to these other factors. Neutral models of this type may help to clarify the poorly understood role of nonselective factors in evolutionary innovation and directionality.

show abstract

Scrambled actin I gene in the micronucleus of Oxytricha nova

Cited by 65 publications

References 7 publications

Volatility of Internal Eliminated Segments in Germ Line Genes of Hypotrichous Ciliates

Volatility of Internal Eliminated Segments in Germ Line Genes of Hypotrichous Ciliates

Evolution of IESs and scrambling in the actin I gene in hypotrichous ciliates

On the Possibility of Constructive Neutral Evolution

Contact Info

Product

Resources

About