The evolution of the novel Sdic gene cluster in Drosophila melanogaster

Ponce, Rita; Hartl, Daniel L.

doi:10.1016/j.gene.2006.02.011

Cited by 22 publications

(25 citation statements)

References 36 publications

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“…This is surprising since segmental duplications disrupt synteny and thereby risk separating extragenic cis-regulatory sequences from their target genes. Nevertheless, some reports have described cases where tandemly duplicated genes have retained the same cis-regulation as their parental copy (e.g., Ponce and Hartl 2006). We do not observe this trend in fugu, but this may be caused by the paucity of segmentally duplicated genes in the fugu genome (155 fugu genes vs. 792 mouse genes and 1967 zebrafish genes).…”

Section: Conserved Noncoding Sequences Are Strongly Associated With Gcontrasting

confidence: 86%

Deeply conserved chordate noncoding sequences preserve genome synteny but do not drive gene duplicate retention

et al. 2009

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Animal genomes possess highly conserved cis-regulatory sequences that are often found near genes that regulate transcription and development. Researchers have proposed that the strong conservation of these sequences may affect the evolution of the surrounding genome, both by repressing rearrangement, and possibly by promoting duplicate gene retention. Conflicting data, however, have made the validity of these propositions unclear. Here, we use a new computational method to identify phylogenetically conserved noncoding elements (PCNEs) in a manner that is not biased by rearrangement and duplication. This method is powerful enough to identify more than a thousand PCNEs that have been conserved between vertebrates and the basal chordate amphioxus. We test 42 of our PCNEs in transgenic zebrafish assays-including examples from vertebrates and amphioxus-and find that the majority are functional enhancers. We find that PCNEs are enriched around genes with ancient synteny conservation, and that this association is strongest for extragenic PCNEs, suggesting that cis-regulatory interdigitation plays a key role in repressing genome rearrangement. Next, we classify mouse and zebrafish genes according to association with PCNEs, synteny conservation, duplication history, and presence in bidirectional promoter pairs, and use these data to cluster gene functions into a series of distinct evolutionary patterns. These results demonstrate that subfunctionalization of conserved cis-regulation has not been the primary determinate of gene duplicate retention in vertebrates. Instead, the data support the gene balance hypothesis, which proposes that duplicate retention has been driven by selection against dosage imbalances in genes with many protein connections.

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Section: Conserved Noncoding Sequences Are Strongly Associated With Gcontrasting

confidence: 86%

Deeply conserved chordate noncoding sequences preserve genome synteny but do not drive gene duplicate retention

et al. 2009

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“…Sequence comparison of the annotated copies suggests a scenario in which two duplications following the formation of Sdic gave rise to the current molecular organization of the whole multigene family. This event was estimated to have occurred 102-180 thousand years ago (20). Sdic presumably encodes a sperm-specific axonemal dynein intermediate chain.…”

mentioning

confidence: 99%

Functional evidence that a recently evolved Drosophila sperm-specific gene boosts sperm competition

Yeh

Chan

et al. 2012

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

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In many species, both morphological and molecular traits related to sex and reproduction evolve faster in males than in females. Ultimately, rapid male evolution relies on the acquisition of genetic variation associated with differential reproductive success. Many newly evolved genes are associated with novel functions that might enhance male fitness. However, functional evidence of the adaptive role of recently originated genes in males is still lacking. The Sperm dynein intermediate chain multigene family, which encodes a Sperm dynein intermediate chain presumably involved in sperm motility, originated from complex genetic rearrangements in the lineage that leads to Drosophila melanogaster within the last 5.4 million years since its split from Drosophila simulans. We deleted all the members of this multigene family resident on the X chromosome of D. melanogaster by chromosome engineering and found that, although the deletion does not result in a reduction of progeny number, it impairs the competence of the sperm in the presence of sperm from wildtype males. Therefore, the Sperm dynein intermediate chain multigene family contributes to the differential reproductive success among males and illustrates precisely how quickly a new gene function can be incorporated into the genetic network of a species.Faster-male evolution | male fertility

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“…The Sdic cluster is located in the X chromosome of D. melanogaster between the genes Cdic and AnnX; it consists of four tandem copies of a newly evolved gene, the Sdic gene, and was formed by three successive rounds of duplications (Ponce and Hartl 2006). Sdic encodes a novel sperm motility protein and is a chimeric gene formed by duplication, deletions and sequence rearrangements (Nurmisnky et al 1998;Ranz et al 2003).…”

Section: Introductionmentioning

confidence: 99%

“…These elements are 5¢ truncated, indicating that they are DOA, and share the same indel pattern and direct flanking repeats, indicating that they are duplicates. Furthermore, there is evidence that these elements were inserted in this region during the very early steps of the formation of the Sdic cluster and did not have any direct bearing on the duplication events that occurred, but rather they were inconsequential passengers during the duplications that gave rise to this gene cluster (Ponce and Hartl 2006). Their presence in this cluster and the above characteristics, make these non-LTR elements ideal markers to date the duplication events on the origin of this cluster.…”

Section: Introductionmentioning

confidence: 99%

“…Their presence in this cluster and the above characteristics, make these non-LTR elements ideal markers to date the duplication events on the origin of this cluster. The objective of this work was to use the history of the RT1C element to determine the insertion times of RT1C element upon the Sdic gene cluster, check if the chronology of duplications is in accordance with our model for the evolution of the Sdic cluster (Ponce and Hartl 2006), and date the formation of this cluster.…”

Section: Introductionmentioning

confidence: 99%

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The use of a non-LTR element to date the formation of the Sdic gene cluster

Ponce

2007

Genetica

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Transposable elements comprise a considerable part of eukaryotic genomes, and there is increasing evidence for their role in the evolution of genomes. The number of active transposable elements present in the host genome at any given time is probably small relative to the number of elements that no longer transpose. The elements that have lost the ability to transpose tend to evolve neutrally. For example, non-LTR retrotransposons often become 5' truncated due to their own transposition mechanism and hence lose their ability to transpose. The resulting transposons can be characterized as "dead-on-arrival" (DOA) elements. Because they are abundant and ubiquitous, and evolve neutrally in the location where they were inserted, these DOA non-LTR elements make a useful tool to date molecular events. There are four copies of a "dead-on-arrival" RT1C element on the recently formed Sdic gene cluster of Drosophila melanogaster, that are not present in the equivalent region of the other species of the melanogaster subgroup. The life history of the RT1C elements in the genome of D. melanogaster was used to determine the insertion chronology of the elements in the cluster and to date the duplication events that originated this cluster.

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The evolution of the novel Sdic gene cluster in Drosophila melanogaster

Cited by 22 publications

References 36 publications

Deeply conserved chordate noncoding sequences preserve genome synteny but do not drive gene duplicate retention

Deeply conserved chordate noncoding sequences preserve genome synteny but do not drive gene duplicate retention

Functional evidence that a recently evolved Drosophila sperm-specific gene boosts sperm competition

The use of a non-LTR element to date the formation of the Sdic gene cluster

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