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

Hogan, Daniel J.; Hewitt, Elizabeth A.; Orr, Kindra E.; Prescott, David M.; Müller, Kirsten M.

doi:10.1073/pnas.011578598

Cited by 28 publications

(46 citation statements)

References 9 publications

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“…Previous studies of the considerably less-scrambled actin I gene are consistent with an origin of scrambled genes after the divergence of Uroleptus (8) and the oxytrichids from the lineage leading to Urostyla (10). Unlike the DNA pol ␣ gene, none of the early-diverging actin I genes is extensively fragmented.…”

Section: Resultssupporting

confidence: 56%

“…Unlike the DNA pol ␣ gene, none of the early-diverging actin I genes is extensively fragmented. For example, the U. grandis actin I gene possesses only three nonscrambled segments (10), and there are no scrambled intermediate species included in ref. 10.…”

Section: Resultsmentioning

confidence: 99%

“…For example, the U. grandis actin I gene possesses only three nonscrambled segments (10), and there are no scrambled intermediate species included in ref. 10. Therefore, we infer that the DNA pol ␣ gene in U. grandis probably accumulated many new noncoding segments after it diverged, and the less-fragmented gene in Holosticha might resemble the nonscrambled ancestral state of this gene.…”

Section: Resultsmentioning

confidence: 99%

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The evolutionary origin of a complex scrambled gene

Chang

Bryson

Liang

et al. 2005

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

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Some species of ciliates undergo massive DNA elimination and genome rearrangement to construct gene-sized ''chromosomes'' in their somatic nucleus. An example is the extensively scrambled DNA polymerase ␣ gene that is broken into 48 pieces and distributed over two unlinked loci in Stylonychia. To understand the emergence of this complex phenomenon during evolution, we examined DNA polymerase ␣ genes in several earlier diverging species, representing evolutionary intermediates. Mapping these data onto an evolutionary tree suggests that this gene became extensively fragmented and scrambled over evolutionary time through a series of steps, each leading to greater complexity. Our results also suggest a possible mechanism for intron loss by deletion of intron sequences as DNA during development of the somatic nucleus.ciliate ͉ DNA polymerase ͉ hypotrich ͉ intron loss ͉ spirotrich C iliates comprise a diverse group of microbial eukaryotes, or protists. These organisms contain two types of nuclei: a somatic macronucleus that is active during vegetative growth and a germ-line micronucleus that is quiescent except during sexual recombination (1). During sexual conjugation, the two mating cells exchange haploid micronuclei, after which the old macronucleus degrades, and the new diploid micronucleus develops into the new macronucleus. Extensive loss of DNA from the long micronuclear chromosomes, coupled to DNA rearrangement, removes transposons and most intergenic spacer DNA between genes, as well as intragenic spacer DNA, known as internal eliminated segments (IESs). In spirotrichous (formerly hypotrichous) ciliates, the remaining DNA sequences, known as macronuclear destined segments (MDSs), can occupy as little as 2-5% of the germ-line genome. These mostly coding regions assemble together to form Ϸ24,000 types of DNA molecules in the somatic nucleus. Because their average size is just 2.2 kbp and they usually contain only one gene, they are sometimes called ''nano-chromosomes.'' Short telomeres are added to both ends before these molecules are amplified several-thousand-fold (1-3).Furthermore, the germ-line order of the coding regions in 20-30% of the genes in stichotrichous ciliates (a subset of spirotrichous ciliates) are permuted, or scrambled, relative to their linear order in the macronucleus. Although the mechanism of reordering these segments is not well understood, short direct repeats, called pointers, may guide the unscrambling process (1, 4). Invariably, one copy of a repeated word pair is present at the 3Ј end of germ-line segment n and at the 5Ј end of segment n ϩ 1, providing the information to link them together, with only one copy of the repeated word retained in the final DNA molecule (1). Although fragmented genes do occur in other organisms [examples include V(D)J recombination in the vertebrate immune system and split ribosomal RNA genes in the mitochondria of fungi (5) and protists (6, 7)], rarely are they sewn back together at the DNA level.Three different scrambled genes, actin I (8-10), ␣ telomer...

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Section: Resultssupporting

confidence: 56%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

See 1 more Smart Citation

The evolutionary origin of a complex scrambled gene

Chang

Bryson

Liang

et al. 2005

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

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“…In EIF2G IES4, ?1 and ?10 indicate an additional one or ten repeats of the sequence GTTTGT in the A1 alleles relative to the A2 alleles. * represents nine polymorphic sites at this location that are identical in all sequences except CL10 A1 (see Supplement 2) extensively fragmented genomes (e.g., DuBois and Prescott 1997; Hogan et al 2001;Chang et al 2006). …”

Section: Micronuclear Structurementioning

confidence: 99%

Evolution of Germline-Limited Sequences in Two Populations of the Ciliate Chilodonella uncinata

2012

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“…A scheme based on eight stichotrichs has been proposed to explain both the stepwise addition of IESs to the micronuclear actin I gene during evolution, as well as the origin and evolution of MDS scrambling (DuBois and Prescott 1995Hoffman and Prescott 1997;Prescott et al 1998). The micronuclear gene encoding actin I in two of the eight stichotrichs, Urostyla grandis and Engelmanniella mobilis, contains two and three IESs, and hence, three and four MDSs, respectively, and the MDSs are not scrambled (Hogan et al 2001). In the other six stichotrichs the actin I gene contains seven to 11 IESs and hence eight to 12 MDSs, most of which are scrambled in all six organisms.…”

Section: Introductionmentioning

confidence: 97%

The scrambled Actin I gene in Uroleptus pisces

Dalby

Prescott

2004

Chromosoma

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The micronuclear gene encoding actin I in Uroleptus pisces occurs in two segments. Segment I contains 638 bp divided into six macronuclear destined subsegments, or MDSs, by five internal eliminated segments, or IESs. The MDSs in segment 1 are in the scrambled disorder, 1-2-4-8-6-15, with MDSs 8 and 6 inverted. Segment II contains 2452 bp divided into ten MDSs by nine IESs in the scrambled disorder, 3-5-7-10-13-12-9-14-16-11, with MDSs 12, 9, and 11 inverted. Extensive attempts by polymerase chain reaction to connect the two segments failed. We conclude that the two segments are separated by a very long IES or are in different loci. The pattern of the 16 scrambled MDSs is entirely different from the scrambled pattern observed for the actin I gene in six other stichotrichs. We conclude that the actin I gene became scrambled on two separate occasions during stichotrich evolution: once in the lineage leading to the group of six stichotrichs, which includes, among others, Sterkiella species and Stylonychia lemnae, and once in the lineage leading to Uroleptus pisces. Repeated sequence pairs (pointers) of three to 14 bases at the ends of MDSs appear to be essential for correct splicing of MDSs during macronuclear development. However, the micronuclear actin gene also contains 40 matches of eight or more bases between IESs and MDSs that do not function as pointers. To prevent these ectopic repeats from causing improper processing of the micronuclear gene appears to demand a template of DNA or RNA from the old macronucleus to guide splicing of MDSs in the orthodox order.

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

Cited by 28 publications

References 9 publications

The evolutionary origin of a complex scrambled gene

The evolutionary origin of a complex scrambled gene

Evolution of Germline-Limited Sequences in Two Populations of the Ciliate Chilodonella uncinata

The scrambled Actin I gene in Uroleptus pisces

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