Emergence and loss of spliceosomal twin introns

Flipphi, Michel; Fekete, Erzsébet; Karaffa, Levente; Kavalecz, Napsugár; Cerqueira, Gustavo C.; Scazzocchio, Claudio

doi:10.1186/s40694-017-0037-y

Cited by 6 publications

(14 citation statements)

References 31 publications

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“…The first stwintrons we reported on were encountered serendipitously 14,15 . However, these simple, degenerated sequence motifs we designed allowed us to actively search for candidate stwintrons in whole genome sequences: a screen for [D1,2] stwintrons led to the identification of two bona fide stwintrons 16,17 .…”

Section: Methodsmentioning

confidence: 99%

“…The second type consists of intronic sequences in which (one) U2 intron(s) is/are nested within (an)other U2 intron(s) which can be, but not necessarily are, removed sequentially 11–13 . We have described spliceosomal twin introns (“stwintrons”) in fungi 14–17 . These are complex intervening sequences where the “external” intron can only be removed after the excision of the “internal” intron nested within.…”

Section: Introductionmentioning

confidence: 99%

“…We have characterised two of the three possible classes of stwintrons (Fig. 1), those where the internal intron interrupts the donor (named [D] stwintrons) or the acceptor ([A] stwintrons) of the external intron 14–17 . We have not published evidence for the existence of the third class, in which the internal intron disrupts the sequence element around the lariat branchpoint adenosine of the external intron ([L] stwintrons).

Figure 1Structure of the three classes of spliceosomal twin introns.…”

Section: Introductionmentioning

confidence: 99%

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A spliceosomal twin intron (stwintron) participates in both exon skipping and evolutionary exon loss

Kavalecz

Fekete

Karaffa

et al. 2019

Sci Rep

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Spliceosomal twin introns (stwintrons) are introns where any of the three consensus sequences involved in splicing is interrupted by another intron (internal intron). In Aspergillus nidulans , a donor-disrupted stwintron (intron-1) is extant in the transcript encoding a reticulon-like protein. The orthologous transcript of Aspergillus niger can be alternatively spliced; the exon downstream the stwintron could be skipped by excising a sequence that comprises this stwintron, the neighbouring intron-2, and the exon bounded by these. This process involves the use of alternative 3′ splice sites for the internal intron, the resulting alternative intervening sequence being a longer 3′-extended stwintron. In 29 species of Onygenales , a multi-step splicing process occurs in the orthologous transcript, in which a complex intervening sequence including the stwintron and neigbouring intron-2, generates by three splicing reactions a “second order intron” which must then be excised with a fourth splicing event. The gene model in two species can be envisaged as one canonical intron (intron-1) evolved from this complex intervening sequence of nested canonical introns found elsewhere in Onygenales . Postulated splicing intermediates were experimentally verified in one or more species. This work illustrates a role of stwintrons in both alternative splicing and the evolution of intron structure.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Figure 1Structure of the three classes of spliceosomal twin introns.…”

Section: Introductionmentioning

confidence: 99%

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A spliceosomal twin intron (stwintron) participates in both exon skipping and evolutionary exon loss

Kavalecz

Fekete

Karaffa

et al. 2019

Sci Rep

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“…Due to the large variation in intron content across fungal genomes, introns are considered to be one of the more rapidly evolving genomic elements in fungi 58 , 59 , 66 . Spliceosomal twin introns or “stwintrons” were recently identified in several orders of ascomycete species 68 , 69 . These nested introns display intriguing trends of gain and loss across fungi and either are removed by complex, multi-step splicing events or trigger alternative splicing and exon skipping.…”

Section: Small-scale Evolution Of Fungal Genomesmentioning

confidence: 99%

Advances in understanding the evolution of fungal genome architecture

2020

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Diversity within the fungal kingdom is evident from the wide range of morphologies fungi display as well as the various ecological roles and industrial purposes they serve. Technological advances, particularly in long-read sequencing, coupled with the increasing efficiency and decreasing costs across sequencing platforms have enabled robust characterization of fungal genomes. These sequencing efforts continue to reveal the rampant diversity in fungi at the genome level. Here, we discuss studies that have furthered our understanding of fungal genetic diversity and genomic evolution. These studies revealed the presence of both small-scale and large-scale genomic changes. In fungi, research has recently focused on many small-scale changes, such as how hypermutation and allelic transmission impact genome evolution as well as how and why a few specific genomic regions are more susceptible to rapid evolution than others. High-throughput sequencing of a diverse set of fungal genomes has also illuminated the frequency, mechanisms, and impacts of large-scale changes, which include chromosome structural variation and changes in chromosome number, such as aneuploidy, polyploidy, and the presence of supernumerary chromosomes. The studies discussed herein have provided great insight into how the architecture of the fungal genome varies within species and across the kingdom and how modern fungi may have evolved from the last common fungal ancestor and might also pave the way for understanding how genomic diversity has evolved in all domains of life.

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“…Intervening sequences of any of the three main classes -group I, group II and spliceosomal -can be made up of more than one functional intron unit [4][5][6] . Previously, we have described a particular class of nested U2 introns, the stwintron, for which the excision of the internal intron is required to accomplish the subsequent excision of the external intron because the former interrupts one of the three conserved intron splicing elements of the latter, the 5'-donor, the sequence element around the lariat branch point adenosine, or the 3'-acceptor [7][8][9][10][11] (Fig. 1).…”

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Complex intron generation in the yeast genus Lipomyces

Fekete

Kavalecz

Pénzes

et al. 2020

Sci Rep

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In primary transcripts of eukaryotic nuclear genes, coding sequences are often interrupted by U2-type introns. Such intervening sequences can constitute complex introns excised by consecutive splicing reactions. The origin of spliceosomal introns is a vexing problem. Sequence variation existent across fungal taxa provides means to study their structure and evolution. In one class of complex introns called [D] stwintrons, an (internal) U2 intron is nested within the 5'-donor element of another (external) U2 intron. In the gene for a reticulon-like protein in species of the ascomycete yeast genus Lipomyces, the most 5' terminal intron position is occupied by one of three complex intervening sequences consistent of differently nested U2 intron units, as demonstrated in L. lipofer, L. suomiensis, and L. starkeyi. In L. starkeyi, the donor elements of the constituent introns are abutting and the complex intervening sequence can be excised alternatively either with one standard splicing reaction or, as a [D] stwintron, by two consecutive reactions. Our work suggests how [D] stwintrons could emerge by the appearance of new functional splice sites within an extant intron. The stepwise stwintronisation mechanism may involve duplication of the functional intron donor element of the ancestor intron.

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Emergence and loss of spliceosomal twin introns

Cited by 6 publications

References 31 publications

A spliceosomal twin intron (stwintron) participates in both exon skipping and evolutionary exon loss

A spliceosomal twin intron (stwintron) participates in both exon skipping and evolutionary exon loss

Advances in understanding the evolution of fungal genome architecture

Complex intron generation in the yeast genus Lipomyces

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